Publications by authors named "Markus Friedrich"

80 Publications

Correction to: Genome-enabled insights into the biology of thrips as crop pests.

BMC Biol 2020 Nov 16;18(1):169. Epub 2020 Nov 16.

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

An amendment to this paper has been published and can be accessed via the original article.
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http://dx.doi.org/10.1186/s12915-020-00915-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7670811PMC
November 2020

Genomic signatures of globally enhanced gene duplicate accumulation in the megadiverse higher Diptera fueling intralocus sexual conflict resolution.

PeerJ 2020 12;8:e10012. Epub 2020 Oct 12.

Department of Biological Sciences, Wayne State University, Detroit, MI, USA.

Gene duplication is an important source of evolutionary innovation. To explore the relative impact of gene duplication during the diversification of major insect model system lineages, we performed a comparative analysis of lineage-specific gene duplications in the fruit fly (Diptera: Brachycera), the mosquito ae (Diptera: Culicomorpha), the red flour beetle (Coleoptera), and the honeybee (Hymenoptera). Focusing on close to 6,000 insect core gene families containing maximally six paralogs, we detected a conspicuously higher number of lineage-specific duplications in (689) compared to (315), (386), and (223). Based on analyses of sequence divergence, phylogenetic distribution, and gene ontology information, we present evidence that an increased background rate of gene duplicate accumulation played an exceptional role during the diversification of the higher Diptera (Brachycera), in part by providing enriched opportunities for intralocus sexual conflict resolution, which may have boosted speciation rates during the early radiation of the megadiverse brachyceran subclade Schizophora.
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http://dx.doi.org/10.7717/peerj.10012DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7560327PMC
October 2020

Genome-enabled insights into the biology of thrips as crop pests.

BMC Biol 2020 10 19;18(1):142. Epub 2020 Oct 19.

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Background: The western flower thrips, Frankliniella occidentalis (Pergande), is a globally invasive pest and plant virus vector on a wide array of food, fiber, and ornamental crops. The underlying genetic mechanisms of the processes governing thrips pest and vector biology, feeding behaviors, ecology, and insecticide resistance are largely unknown. To address this gap, we present the F. occidentalis draft genome assembly and official gene set.

Results: We report on the first genome sequence for any member of the insect order Thysanoptera. Benchmarking Universal Single-Copy Ortholog (BUSCO) assessments of the genome assembly (size = 415.8 Mb, scaffold N50 = 948.9 kb) revealed a relatively complete and well-annotated assembly in comparison to other insect genomes. The genome is unusually GC-rich (50%) compared to other insect genomes to date. The official gene set (OGS v1.0) contains 16,859 genes, of which ~ 10% were manually verified and corrected by our consortium. We focused on manual annotation, phylogenetic, and expression evidence analyses for gene sets centered on primary themes in the life histories and activities of plant-colonizing insects. Highlights include the following: (1) divergent clades and large expansions in genes associated with environmental sensing (chemosensory receptors) and detoxification (CYP4, CYP6, and CCE enzymes) of substances encountered in agricultural environments; (2) a comprehensive set of salivary gland genes supported by enriched expression; (3) apparent absence of members of the IMD innate immune defense pathway; and (4) developmental- and sex-specific expression analyses of genes associated with progression from larvae to adulthood through neometaboly, a distinct form of maturation differing from either incomplete or complete metamorphosis in the Insecta.

Conclusions: Analysis of the F. occidentalis genome offers insights into the polyphagous behavior of this insect pest that finds, colonizes, and survives on a widely diverse array of plants. The genomic resources presented here enable a more complete analysis of insect evolution and biology, providing a missing taxon for contemporary insect genomics-based analyses. Our study also offers a genomic benchmark for molecular and evolutionary investigations of other Thysanoptera species.
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http://dx.doi.org/10.1186/s12915-020-00862-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7570057PMC
October 2020

Evolutionary conservation of opsin gene expression patterns in the compound eyes of darkling beetles.

Dev Genes Evol 2020 11 2;230(5-6):339-345. Epub 2020 Oct 2.

Department of Biological Sciences, Wayne State University, 5047 Gullen Mall, Detroit, MI, 48202, USA.

Recent large-scale studies of opsin gene contents in representatives of the largest order of insects, the Coleoptera (beetles), revealed that the blue wavelength-sensitive (B) opsin subfamily is absent in this clade, while the ultraviolet- (UV) and long wavelength-sensitive (LW) opsin subfamilies are broadly conserved with gene duplications possibly reintroducing blue sensitivity in select subclades. Little is known yet, however, how opsin genes are expressed in the compound eyes of beetles. In a previous study, we analyzed opsin gene expression in the red flour beetle Tribolium castaneum, a member of the family of darkling beetles (Tenebrionidae), and found that a singleton LW opsin homolog is homogeneously expressed in all photoreceptors of the compound eye retina with a singleton UV opsin homolog being co-expressed in the R7 subtype photoreceptors. To probe for the evolutionary conservation of these expression patterns, we isolated complete opsin transcript sequences from three additional species in the subfamily Tenebrionidae (Tribolium confusum, Tenebrio molitor, Zophobas morio) and studied their expression via whole mount in situ hybridization in the pupal retina. These experiments revealed very similar, if not identical, photoreceptor subtype-specific expression patterns in all three species compared with T. castaneum. Documenting a deep conservation of photoreceptor subtype-specific opsin gene expression in this range of darkling beetles, our study provides a first point of reference for broader comparative studies of retinal organization in the Coleoptera.
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http://dx.doi.org/10.1007/s00427-020-00669-2DOI Listing
November 2020

Towards reconstructing the dipteran demise of an ancient essential gene: E3 ubiquitin ligase Murine double minute.

Dev Genes Evol 2020 07 4;230(4):279-294. Epub 2020 Jul 4.

Department of Biological Sciences, Wayne State University, 5047 Gullen Mall, Detroit, MI, 48202, USA.

Genome studies have uncovered many examples of essential gene loss, raising the question of how ancient genes transition from essentiality to dispensability. We explored this process for the deeply conserved E3 ubiquitin ligase Murine double minute (Mdm), which is lacking in Drosophila despite the conservation of its main regulatory target, the cellular stress response gene p53. Conducting gene expression and knockdown experiments in the red flour beetle Tribolium castaneum, we found evidence that Mdm has remained essential in insects where it is present. Using bioinformatics approaches, we confirm the absence of the Mdm gene family in Drosophila, mapping its loss to the stem lineage of schizophoran Diptera and Pipunculidae (big-headed flies), about 95-85 million years ago. Intriguingly, this gene loss event was preceded by the de novo origin of the gene Companion of reaper (Corp), a novel p53 regulatory factor that is characterized by functional similarities to vertebrate Mdm2 despite lacking E3 ubiquitin ligase protein domains. Speaking against a 1:1 compensatory gene gain/loss scenario, however, we found that hoverflies (Syrphidae) and pointed-wing flies (Lonchopteridae) possess both Mdm and Corp. This implies that the two p53 regulators have been coexisting for ~ 150 million years in select dipteran clades and for at least 50 million years in the lineage to Schizophora and Pipunculidae. Given these extensive time spans of Mdm/Corp coexistence, we speculate that the loss of Mdm in the lineage to Drosophila involved further acquisitions of compensatory gene activities besides the emergence of Corp. Combined with the previously noted reduction of an ancestral P53 contact domain in the Mdm homologs of crustaceans and insects, we conclude that the loss of the ancient Mdm gene family in flies was the outcome of incremental functional regression over long macroevolutionary time scales.
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http://dx.doi.org/10.1007/s00427-020-00663-8DOI Listing
July 2020

The brachyceran de novo gene PIP82, a phosphorylation target of aPKC, is essential for proper formation and maintenance of the rhabdomeric photoreceptor apical domain in Drosophila.

PLoS Genet 2020 06 24;16(6):e1008890. Epub 2020 Jun 24.

Department of Biological Sciences, Wayne State University, Detroit, Michigan, United States of America.

The Drosophila apical photoreceptor membrane is defined by the presence of two distinct morphological regions, the microvilli-based rhabdomere and the stalk membrane. The subdivision of the apical membrane contributes to the geometrical positioning and the stereotypical morphology of the rhabdomeres in compound eyes with open rhabdoms and neural superposition. Here we describe the characterization of the photoreceptor specific protein PIP82. We found that PIP82's subcellular localization demarcates the rhabdomeric portion of the apical membrane. We further demonstrate that PIP82 is a phosphorylation target of aPKC. PIP82 localization is modulated by phosphorylation, and in vivo, the loss of the aPKC/Crumbs complex results in an expansion of the PIP82 localization domain. The absence of PIP82 in photoreceptors leads to misshapped rhabdomeres as a result of misdirected cellular trafficking of rhabdomere proteins. Comparative analyses reveal that PIP82 originated de novo in the lineage leading to brachyceran Diptera, which is also characterized by the transition from fused to open rhabdoms. Taken together, these findings define a novel factor that delineates and maintains a specific apical membrane domain, and offers new insights into the functional organization and evolutionary history of the Drosophila retina.
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http://dx.doi.org/10.1371/journal.pgen.1008890DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7340324PMC
June 2020

Sawfly Genomes Reveal Evolutionary Acquisitions That Fostered the Mega-Radiation of Parasitoid and Eusocial Hymenoptera.

Genome Biol Evol 2020 07;12(7):1099-1188

Department of Evolutionary Biology and Ecology, Institute of Biology I (Zoology), Albert Ludwig University Freiburg, Germany.

The tremendous diversity of Hymenoptera is commonly attributed to the evolution of parasitoidism in the last common ancestor of parasitoid sawflies (Orussidae) and wasp-waisted Hymenoptera (Apocrita). However, Apocrita and Orussidae differ dramatically in their species richness, indicating that the diversification of Apocrita was promoted by additional traits. These traits have remained elusive due to a paucity of sawfly genome sequences, in particular those of parasitoid sawflies. Here, we present comparative analyses of draft genomes of the primarily phytophagous sawfly Athalia rosae and the parasitoid sawfly Orussus abietinus. Our analyses revealed that the ancestral hymenopteran genome exhibited traits that were previously considered unique to eusocial Apocrita (e.g., low transposable element content and activity) and a wider gene repertoire than previously thought (e.g., genes for CO2 detection). Moreover, we discovered that Apocrita evolved a significantly larger array of odorant receptors than sawflies, which could be relevant to the remarkable diversification of Apocrita by enabling efficient detection and reliable identification of hosts.
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http://dx.doi.org/10.1093/gbe/evaa106DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7455281PMC
July 2020

Brown marmorated stink bug, Halyomorpha halys (Stål), genome: putative underpinnings of polyphagy, insecticide resistance potential and biology of a top worldwide pest.

BMC Genomics 2020 Mar 14;21(1):227. Epub 2020 Mar 14.

USDA-ARS Invasive Insect Biocontrol and Behavior Laboratory, Beltsville, MD, 20705, USA.

Background: Halyomorpha halys (Stål), the brown marmorated stink bug, is a highly invasive insect species due in part to its exceptionally high levels of polyphagy. This species is also a nuisance due to overwintering in human-made structures. It has caused significant agricultural losses in recent years along the Atlantic seaboard of North America and in continental Europe. Genomic resources will assist with determining the molecular basis for this species' feeding and habitat traits, defining potential targets for pest management strategies.

Results: Analysis of the 1.15-Gb draft genome assembly has identified a wide variety of genetic elements underpinning the biological characteristics of this formidable pest species, encompassing the roles of sensory functions, digestion, immunity, detoxification and development, all of which likely support H. halys' capacity for invasiveness. Many of the genes identified herein have potential for biomolecular pesticide applications.

Conclusions: Availability of the H. halys genome sequence will be useful for the development of environmentally friendly biomolecular pesticides to be applied in concert with more traditional, synthetic chemical-based controls.
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http://dx.doi.org/10.1186/s12864-020-6510-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7071726PMC
March 2020

Gene content evolution in the arthropods.

Genome Biol 2020 01 23;21(1):15. Epub 2020 Jan 23.

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Background: Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods.

Results: Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception.

Conclusions: These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.
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http://dx.doi.org/10.1186/s13059-019-1925-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6977273PMC
January 2020

Enhanced genome assembly and a new official gene set for Tribolium castaneum.

BMC Genomics 2020 Jan 14;21(1):47. Epub 2020 Jan 14.

Georg-August-Universität Göttingen, Göttingen, Germany.

Background: The red flour beetle Tribolium castaneum has emerged as an important model organism for the study of gene function in development and physiology, for ecological and evolutionary genomics, for pest control and a plethora of other topics. RNA interference (RNAi), transgenesis and genome editing are well established and the resources for genome-wide RNAi screening have become available in this model. All these techniques depend on a high quality genome assembly and precise gene models. However, the first version of the genome assembly was generated by Sanger sequencing, and with a small set of RNA sequence data limiting annotation quality.

Results: Here, we present an improved genome assembly (Tcas5.2) and an enhanced genome annotation resulting in a new official gene set (OGS3) for Tribolium castaneum, which significantly increase the quality of the genomic resources. By adding large-distance jumping library DNA sequencing to join scaffolds and fill small gaps, the gaps in the genome assembly were reduced and the N50 increased to 4753kbp. The precision of the gene models was enhanced by the use of a large body of RNA-Seq reads of different life history stages and tissue types, leading to the discovery of 1452 novel gene sequences. We also added new features such as alternative splicing, well defined UTRs and microRNA target predictions. For quality control, 399 gene models were evaluated by manual inspection. The current gene set was submitted to Genbank and accepted as a RefSeq genome by NCBI.

Conclusions: The new genome assembly (Tcas5.2) and the official gene set (OGS3) provide enhanced genomic resources for genetic work in Tribolium castaneum. The much improved information on transcription start sites supports transgenic and gene editing approaches. Further, novel types of information such as splice variants and microRNA target genes open additional possibilities for analysis.
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http://dx.doi.org/10.1186/s12864-019-6394-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6961396PMC
January 2020

Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes.

Genome Biol 2019 09 2;20(1):187. Epub 2019 Sep 2.

Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA.

Background: Tsetse flies (Glossina sp.) are the vectors of human and animal trypanosomiasis throughout sub-Saharan Africa. Tsetse flies are distinguished from other Diptera by unique adaptations, including lactation and the birthing of live young (obligate viviparity), a vertebrate blood-specific diet by both sexes, and obligate bacterial symbiosis. This work describes the comparative analysis of six Glossina genomes representing three sub-genera: Morsitans (G. morsitans morsitans, G. pallidipes, G. austeni), Palpalis (G. palpalis, G. fuscipes), and Fusca (G. brevipalpis) which represent different habitats, host preferences, and vectorial capacity.

Results: Genomic analyses validate established evolutionary relationships and sub-genera. Syntenic analysis of Glossina relative to Drosophila melanogaster shows reduced structural conservation across the sex-linked X chromosome. Sex-linked scaffolds show increased rates of female-specific gene expression and lower evolutionary rates relative to autosome associated genes. Tsetse-specific genes are enriched in protease, odorant-binding, and helicase activities. Lactation-associated genes are conserved across all Glossina species while male seminal proteins are rapidly evolving. Olfactory and gustatory genes are reduced across the genus relative to other insects. Vision-associated Rhodopsin genes show conservation of motion detection/tracking functions and variance in the Rhodopsin detecting colors in the blue wavelength ranges.

Conclusions: Expanded genomic discoveries reveal the genetics underlying Glossina biology and provide a rich body of knowledge for basic science and disease control. They also provide insight into the evolutionary biology underlying novel adaptations and are relevant to applied aspects of vector control such as trap design and discovery of novel pest and disease control strategies.
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http://dx.doi.org/10.1186/s13059-019-1768-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6721284PMC
September 2019

Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome.

Genome Biol 2019 04 2;20(1):64. Epub 2019 Apr 2.

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Background: The Hemiptera (aphids, cicadas, and true bugs) are a key insect order, with high diversity for feeding ecology and excellent experimental tractability for molecular genetics. Building upon recent sequencing of hemipteran pests such as phloem-feeding aphids and blood-feeding bed bugs, we present the genome sequence and comparative analyses centered on the milkweed bug Oncopeltus fasciatus, a seed feeder of the family Lygaeidae.

Results: The 926-Mb Oncopeltus genome is well represented by the current assembly and official gene set. We use our genomic and RNA-seq data not only to characterize the protein-coding gene repertoire and perform isoform-specific RNAi, but also to elucidate patterns of molecular evolution and physiology. We find ongoing, lineage-specific expansion and diversification of repressive C2H2 zinc finger proteins. The discovery of intron gain and turnover specific to the Hemiptera also prompted the evaluation of lineage and genome size as predictors of gene structure evolution. Furthermore, we identify enzymatic gains and losses that correlate with feeding biology, particularly for reductions associated with derived, fluid nutrition feeding.

Conclusions: With the milkweed bug, we now have a critical mass of sequenced species for a hemimetabolous insect order and close outgroup to the Holometabola, substantially improving the diversity of insect genomics. We thereby define commonalities among the Hemiptera and delve into how hemipteran genomes reflect distinct feeding ecologies. Given Oncopeltus's strength as an experimental model, these new sequence resources bolster the foundation for molecular research and highlight technical considerations for the analysis of medium-sized invertebrate genomes.
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http://dx.doi.org/10.1186/s13059-019-1660-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6444547PMC
April 2019

Investigation of Fluorine and Nitrogen as Anionic Dopants in Nickel-Rich Cathode Materials for Lithium-Ion Batteries.

ACS Appl Mater Interfaces 2018 Dec 14;10(51):44452-44462. Epub 2018 Dec 14.

Institute of Physical Chemistry & Center for Materials Research , Justus-Liebig-University Giessen , Heinrich-Buff-Ring 17 , D-35392 Giessen , Germany.

Advanced lithium-ion batteries are of great interest for consumer electronics and electric vehicle applications; however, they still suffer from drawbacks stemming from cathode active material limitations (e.g., insufficient capacities and capacity fading). One approach for alleviating such limitations and stabilizing the active material structure may be anion doping. In this work, fluorine and nitrogen are investigated as potential dopants in Li(NiCoMn)O (NCM) as a prototypical nickel-rich cathode active material. Nitrogen doping is achieved by ammonia treatment of NCM in the presence of oxygen, which serves as an unconventional and new approach. The crystal structure was investigated by means of Rietveld and pair distribution function analysis of X-ray diffraction data, which provide very precise information regarding both the average and local structure, respectively. Meanwhile, time-of-flight secondary-ion mass spectroscopy was used to assess the efficacy of dopant incorporation within the NCM structure. Moreover, scanning electron microscopy and scanning transmission electron microscopy were conducted to thoroughly investigate the dopant influences on the NCM morphology. Finally, the electrochemical performance was tested via galvanostatic cycling of half- and full-cells between 0.1 and 2 C. Ultimately, a dopant-dependent modulation of the NCM structure was found to enable the enhancement of the electrochemical performance, thereby opening a route to cathode active material optimization.
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http://dx.doi.org/10.1021/acsami.8b16049DOI Listing
December 2018

The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water.

BMC Genomics 2018 Nov 21;19(1):832. Epub 2018 Nov 21.

Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, Ecole Normale Supérieure de Lyon 46, allée d'Italie, 69364, Lyon Cedex 07, France.

Background: Having conquered water surfaces worldwide, the semi-aquatic bugs occupy ponds, streams, lakes, mangroves, and even open oceans. The diversity of this group has inspired a range of scientific studies from ecology and evolution to developmental genetics and hydrodynamics of fluid locomotion. However, the lack of a representative water strider genome hinders our ability to more thoroughly investigate the molecular mechanisms underlying the processes of adaptation and diversification within this group.

Results: Here we report the sequencing and manual annotation of the Gerris buenoi (G. buenoi) genome; the first water strider genome to be sequenced thus far. The size of the G. buenoi genome is approximately 1,000 Mb, and this sequencing effort has recovered 20,949 predicted protein-coding genes. Manual annotation uncovered a number of local (tandem and proximal) gene duplications and expansions of gene families known for their importance in a variety of processes associated with morphological and physiological adaptations to a water surface lifestyle. These expansions may affect key processes associated with growth, vision, desiccation resistance, detoxification, olfaction and epigenetic regulation. Strikingly, the G. buenoi genome contains three insulin receptors, suggesting key changes in the rewiring and function of the insulin pathway. Other genomic changes affecting with opsin genes may be associated with wavelength sensitivity shifts in opsins, which is likely to be key in facilitating specific adaptations in vision for diverse water habitats.

Conclusions: Our findings suggest that local gene duplications might have played an important role during the evolution of water striders. Along with these findings, the sequencing of the G. buenoi genome now provides us the opportunity to pursue exciting research opportunities to further understand the genomic underpinnings of traits associated with the extreme body plan and life history of water striders.
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http://dx.doi.org/10.1186/s12864-018-5163-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6249893PMC
November 2018

Massive parallel expansions of Methuselah/Methuselah-like receptors in schizophoran Diptera.

J Exp Zool B Mol Dev Evol 2018 09 29;330(6-7):384-389. Epub 2018 Jul 29.

Department of Biological Sciences, Wayne State University, Detroit, Michigan.

The Methuselah/Methuselah-like (Mth/Mthl) family of G-protein coupled receptors (GPCRs) is represented by 16 homologs in the fruit fly Drosophila melanogaster. Three of them have thus far been functionally characterized and found to play critical roles in cell adhesion, immunity, lifespan, and oxidative stress regulation. Evolutionary studies have shown that the large number of D. melanogaster Mth/Mthl GPCRs arose by at least two rounds of gene duplications. The first produced the "mth superclade" subfamily and was followed by the expansion of the "melanogaster subgroup" cluster within the "mth superclade" of Mth/Mthl GPCRs. The adaptive significance of the Mth/Mthl receptor repertoire expansion in Drosophila remains elusive. Studying the Mth/Mthl gene family content in newly available dipteran genomes, we find that the first expansion of the mthl superclade predates the diversification of schizophoran Diptera approximately 65 million years ago. Unexpectedly, we further find that the subsequent expansion of the melanogaster subgroup cluster was paralleled by independent mth superclade Mth/Mthl GPCR expansions in other schizophoran clades (Muscidae and Tephritidae). Our study thus reveals an even more dynamic diversification of mth superclade GPCRs than previously appreciated and linked to the emergence of schizophoran flies, the most dramatic radiation in the dipteran tree of life.
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http://dx.doi.org/10.1002/jez.b.22813DOI Listing
September 2018

The Toxicogenome of Hyalella azteca: A Model for Sediment Ecotoxicology and Evolutionary Toxicology.

Environ Sci Technol 2018 05 24;52(10):6009-6022. Epub 2018 Apr 24.

Human Genome Sequencing Center , Baylor College of Medicine , Houston , Texas 77030 United States.

Hyalella azteca is a cryptic species complex of epibenthic amphipods of interest to ecotoxicology and evolutionary biology. It is the primary crustacean used in North America for sediment toxicity testing and an emerging model for molecular ecotoxicology. To provide molecular resources for sediment quality assessments and evolutionary studies, we sequenced, assembled, and annotated the genome of the H. azteca U.S. Lab Strain. The genome quality and completeness is comparable with other ecotoxicological model species. Through targeted investigation and use of gene expression data sets of H. azteca exposed to pesticides, metals, and other emerging contaminants, we annotated and characterized the major gene families involved in sequestration, detoxification, oxidative stress, and toxicant response. Our results revealed gene loss related to light sensing, but a large expansion in chemoreceptors, likely underlying sensory shifts necessary in their low light habitats. Gene family expansions were also noted for cytochrome P450 genes, cuticle proteins, ion transporters, and include recent gene duplications in the metal sequestration protein, metallothionein. Mapping of differentially expressed transcripts to the genome significantly increased the ability to functionally annotate toxicant responsive genes. The H. azteca genome will greatly facilitate development of genomic tools for environmental assessments and promote an understanding of how evolution shapes toxicological pathways with implications for environmental and human health.
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http://dx.doi.org/10.1021/acs.est.8b00837DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6091588PMC
May 2018

A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae).

Sci Rep 2018 01 31;8(1):1931. Epub 2018 Jan 31.

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas, USA.

The Colorado potato beetle is one of the most challenging agricultural pests to manage. It has shown a spectacular ability to adapt to a variety of solanaceaeous plants and variable climates during its global invasion, and, notably, to rapidly evolve insecticide resistance. To examine evidence of rapid evolutionary change, and to understand the genetic basis of herbivory and insecticide resistance, we tested for structural and functional genomic changes relative to other arthropod species using genome sequencing, transcriptomics, and community annotation. Two factors that might facilitate rapid evolutionary change include transposable elements, which comprise at least 17% of the genome and are rapidly evolving compared to other Coleoptera, and high levels of nucleotide diversity in rapidly growing pest populations. Adaptations to plant feeding are evident in gene expansions and differential expression of digestive enzymes in gut tissues, as well as expansions of gustatory receptors for bitter tasting. Surprisingly, the suite of genes involved in insecticide resistance is similar to other beetles. Finally, duplications in the RNAi pathway might explain why Leptinotarsa decemlineata has high sensitivity to dsRNA. The L. decemlineata genome provides opportunities to investigate a broad range of phenotypes and to develop sustainable methods to control this widely successful pest.
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http://dx.doi.org/10.1038/s41598-018-20154-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5792627PMC
January 2018

Ancient genetic redundancy of eyeless and twin of eyeless in the arthropod ocular segment.

Authors:
Markus Friedrich

Dev Biol 2017 12 6;432(1):192-200. Epub 2017 Oct 6.

Department of Biological Sciences, Wayne State University, 5047 Gullen Mall, Detroit, MI 48202, USA; Department of Anatomy and Cell Biology, Wayne State University, School of Medicine, 540 East Canfield Avenue, Detroit, MI 48201,USA. Electronic address:

Pax6 transcription factors are essential upstream regulators in the developing anterior brain and peripheral visual system of most bilaterian animals. While a single homolog is in charge of these functions in vertebrates, two Pax6 genes are in Drosophila: eyeless (ey) and twin of eyeless (toy). At first glance, their co-existence seems sufficiently explained by their differential involvement in the specification of two types of insect visual organs: the lateral compound eyes (ey) and the dorsal ocelli (toy). Less straightforward to understand, however, is their genetic redundancy in promoting defined early and late growth phases of the precursor tissue to these organs: the eye-antennal imaginal disc. Drawing on comparative sequence, expression, and gene function evidence, I here conclude that this gene regulatory network module dates back to the dawn of arthropod evolution, securing the embryonic development of the ocular head segment. Thus, ey and toy constitute a paradigm to explore the organization and functional significance of longterm conserved genetic redundancy of duplicated genes. Indeed, as first steps in this direction, recent studies uncovered the shared use of binding sites in shared enhancers of target genes that are under redundant (string) and, strikingly, even subfunctionalized control by ey and toy (atonal). Equally significant, the evolutionarily recent and paralog-specific function of ey to repress the transcription of the antenna fate regulator Distal-less offers a functionally and phylogenetically well-defined opportunity to study the reconciliation of shared, partitioned, and newly acquired functions in a duplicated developmental gene pair.
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http://dx.doi.org/10.1016/j.ydbio.2017.10.001DOI Listing
December 2017

Erratum to: The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species.

Genome Biol 2017 01 18;18(1):11. Epub 2017 Jan 18.

USDA-ARS, Center for Medical, Agricultural and Veterinary Entomology, 1700 S.W. 23rd Drive, Gainesville, FL, 32608, USA.

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http://dx.doi.org/10.1186/s13059-017-1155-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5241912PMC
January 2017

Gene Ages, Nomenclatures, and Functional Diversification of the Methuselah/Methuselah-Like GPCR Family in Drosophila and Tribolium.

J Exp Zool B Mol Dev Evol 2016 12 11;326(8):453-463. Epub 2017 Jan 11.

Advaxis, Inc, Princeton, New Jersey.

Affecting lifespan regulation and oxidative stress resistance, the G-protein coupled receptor (GPCR) gene methuselah (mth) plays important roles in the life history of Drosophila melanogaster. Substantial progress has been made in elucidating the molecular pathways by which mth affects these traits, yet conflicting ideas exist as to how old these genetic interactions are as well as how old the mth gene itself is. Root to these issues is the complex gene family history of the Mth/Mthl GPCR family, which experienced independent expansions in a variety of animal clades, leading to at least six subfamilies in insects. Within insects, drosophilid flies stand out by possessing up to three times more Mth/Mthl receptors due to the expansion of a single subfamily, the mth superclade subfamily, which contains an even younger subfamily introduced here as the melanogaster subgroup subfamily. As a result, most of the 16 Mth/Mthl receptors of D. melanogaster are characterized by n:1 orthology relationships to singleton mth superclade homologs in nondrosophilid species. This challenge is exacerbated by the inconsistent naming of Mth/Mthl orthologs across species. To consolidate this situation, we review established ortholog relationships among insect Mth/Mthl receptors, clarify the gene nomenclatures in two important satellite model species, the fruit fly relative D. virilis and the red flour beetle Tribolium castaneum, and discuss the genetic and functional evolution of the D. melanogaster Mth GPCR.
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http://dx.doi.org/10.1002/jez.b.22721DOI Listing
December 2016

Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle-plant interface.

Genome Biol 2016 11 11;17(1):227. Epub 2016 Nov 11.

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Background: Relatively little is known about the genomic basis and evolution of wood-feeding in beetles. We undertook genome sequencing and annotation, gene expression assays, studies of plant cell wall degrading enzymes, and other functional and comparative studies of the Asian longhorned beetle, Anoplophora glabripennis, a globally significant invasive species capable of inflicting severe feeding damage on many important tree species. Complementary studies of genes encoding enzymes involved in digestion of woody plant tissues or detoxification of plant allelochemicals were undertaken with the genomes of 14 additional insects, including the newly sequenced emerald ash borer and bull-headed dung beetle.

Results: The Asian longhorned beetle genome encodes a uniquely diverse arsenal of enzymes that can degrade the main polysaccharide networks in plant cell walls, detoxify plant allelochemicals, and otherwise facilitate feeding on woody plants. It has the metabolic plasticity needed to feed on diverse plant species, contributing to its highly invasive nature. Large expansions of chemosensory genes involved in the reception of pheromones and plant kairomones are consistent with the complexity of chemical cues it uses to find host plants and mates.

Conclusions: Amplification and functional divergence of genes associated with specialized feeding on plants, including genes originally obtained via horizontal gene transfer from fungi and bacteria, contributed to the addition, expansion, and enhancement of the metabolic repertoire of the Asian longhorned beetle, certain other phytophagous beetles, and to a lesser degree, other phytophagous insects. Our results thus begin to establish a genomic basis for the evolutionary success of beetles on plants.
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http://dx.doi.org/10.1186/s13059-016-1088-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5105290PMC
November 2016

Distinct regulation of atonal in a visual organ of Drosophila: Organ-specific enhancer and lack of autoregulation in the larval eye.

Dev Biol 2017 Jan 29;421(1):67-76. Epub 2016 Sep 29.

Department of Ophthalmology and Center for Vision Research, SUNY Upstate Medical University, Syracuse, NY, USA; Departments of Neuroscience & Physiology and Biochemistry & Molecular Biology, SUNY Upstate Medical University, Syracuse, NY, USA. Electronic address:

Drosophila has three types of visual organs, the larval eyes or Bolwig's organs (BO), the ocelli (OC) and the compound eyes (CE). In all, the bHLH protein Atonal (Ato) functions as the proneural factor for photoreceptors and effects the transition from progenitor cells to differentiating neurons. In this work, we investigate the regulation of ato expression in the BO primordium (BOP). Surprisingly, we find that ato transcription in the BOP is entirely independent of the shared regulatory DNA for the developing CE and OC. The core enhancer for BOP expression, ato, lies ~6kb upstream of the ato gene, in contrast to the downstream location of CE and OC regulatory elements. Moreover, maintenance of ato expression in the neuronal precursors through autoregulation-a common and ancient feature of ato expression that is well-documented in eyes, ocelli and chordotonal organs-does not occur in the BO. We also show that the ato enhancer contains two binding sites for the transcription factor Sine oculis (So), a core component of the progenitor specification network in all three visual organs. These binding sites function in vivo and are specifically bound by So in vitro. Taken together, our findings reveal that the control of ato transcription in the evolutionarily derived BO has diverged considerably from ato regulation in the more ancestral compound eyes and ocelli, to the extent of acquiring what appears to be a distinct and evolutionarily novel cis-regulatory module.
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http://dx.doi.org/10.1016/j.ydbio.2016.09.023DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5358805PMC
January 2017

The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species.

Genome Biol 2016 09 22;17(1):192. Epub 2016 Sep 22.

USDA-ARS, Center for Medical, Agricultural, and Veterinary Entomology, 1700 S.W. 23rd Drive, Gainesville, FL, 32608, USA.

Background: The Mediterranean fruit fly (medfly), Ceratitis capitata, is a major destructive insect pest due to its broad host range, which includes hundreds of fruits and vegetables. It exhibits a unique ability to invade and adapt to ecological niches throughout tropical and subtropical regions of the world, though medfly infestations have been prevented and controlled by the sterile insect technique (SIT) as part of integrated pest management programs (IPMs). The genetic analysis and manipulation of medfly has been subject to intensive study in an effort to improve SIT efficacy and other aspects of IPM control.

Results: The 479 Mb medfly genome is sequenced from adult flies from lines inbred for 20 generations. A high-quality assembly is achieved having a contig N50 of 45.7 kb and scaffold N50 of 4.06 Mb. In-depth curation of more than 1800 messenger RNAs shows specific gene expansions that can be related to invasiveness and host adaptation, including gene families for chemoreception, toxin and insecticide metabolism, cuticle proteins, opsins, and aquaporins. We identify genes relevant to IPM control, including those required to improve SIT.

Conclusions: The medfly genome sequence provides critical insights into the biology of one of the most serious and widespread agricultural pests. This knowledge should significantly advance the means of controlling the size and invasive potential of medfly populations. Its close relationship to Drosophila, and other insect species important to agriculture and human health, will further comparative functional and structural studies of insect genomes that should broaden our understanding of gene family evolution.
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http://dx.doi.org/10.1186/s13059-016-1049-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5034548PMC
September 2016

Shared and distinct mechanisms of atonal regulation in Drosophila ocelli and compound eyes.

Dev Biol 2016 10 23;418(1):10-16. Epub 2016 Aug 23.

Department of Ophthalmology and Center for Vision Research, SUNY Upstate Medical University, Syracuse, NY 13210, USA; Department of Neuroscience & Physiology, SUNY Upstate Medical University, Syracuse, NY 13210, USA; Department of Biochemistry & Molecular Biology, SUNY Upstate Medical University, Syracuse, NY 13210, USA. Electronic address:

The fruit fly Drosophila melanogaster has two types of external visual organs, a pair of compound eyes and a group of three ocelli. At the time of neurogenesis, the proneural transcription factor Atonal mediates the transition from progenitor cells to differentiating photoreceptor neurons in both organs. In the developing compound eye, atonal (ato) expression is directly induced by transcriptional regulators that confer retinal identity, the Retinal Determination (RD) factors. Little is known, however, about control of ato transcription in the ocelli. Here we show that a 2kb genomic DNA fragment contains distinct and common regulatory elements necessary for ato induction in compound eyes and ocelli. The three binding sites that mediate direct regulation by the RD factors Sine oculis and Eyeless in the compound eye are also required in the ocelli. However, in the latter, these sites mediate control by Sine oculis and the other Pax6 factor of Drosophila, Twin of eyeless, which can bind the Pax6 sites in vitro. Moreover, the three sites are differentially utilized in the ocelli: all three are similarly essential for atonal induction in the posterior ocelli, but show considerable redundancy in the anterior ocellus. Strikingly, this difference parallels the distinct control of ato transcription in the posterior and anterior progenitors of the developing compound eyes. From a comparative perspective, our findings suggest that the ocelli of arthropods may have originated through spatial partitioning from the dorsal edge of an ancestral compound eye.
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http://dx.doi.org/10.1016/j.ydbio.2016.08.025DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5223745PMC
October 2016

Ancient default activators of terminal photoreceptor differentiation in the pancrustacean compound eye: the homeodomain transcription factors Otd and Pph13.

Curr Opin Insect Sci 2016 02 14;13:33-42. Epub 2015 Nov 14.

Department of Biology, Indiana University, Bloomington, IN 47405, USA.

The origin of the Drosophila compound eye predates the ancestor of Pancrustacea, the arthropod clade that includes insects and Crustaceans. Recent studies in emerging model systems for pancrustacean development-the red flour beetle Tribolium castaneum and water flea Daphnia pulex-have begun to shed light on the evolutionary conservation of transcriptional mechanisms found for the Drosophila compound eye. Here, we discuss the conserved roles of the transcription factors Otd and Pph13, which complement each other in two terminal events of photoreceptor differentiation: rhabdomere morphogenesis and transcriptional default activation of opsin gene expression. The synthesis of these data allows us to frame an evolutionary developmental model of the earliest events that generated the wavelength-specific photoreceptor subtypes of pancrustacean compound eyes.
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http://dx.doi.org/10.1016/j.cois.2015.10.006DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5221501PMC
February 2016

Topical antifungal-corticosteroid combination therapy for the treatment of superficial mycoses: conclusions of an expert panel meeting.

Mycoses 2016 Jun 24;59(6):365-73. Epub 2016 Feb 24.

Department of Pathophysiology and Transplantation, Universita degli Studi di Milano, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Foundation, Cà Granda Ospedale Maggiore Policlinico, Milan, Italy.

Superficial fungal infections affect 20-25% of people worldwide and can cause considerable morbidity, particularly if an inflammatory component is present. As superficial fungal infections can be diverse, the treatment should be tailored to the individual needs of the patient and several factors should be taken into account when deciding on the most appropriate treatment option. These include the type, location and surface area of the infection, patient age, degree of inflammation and underlying comorbidities. Although several meta-analyses have shown that there are no significant differences between the numerous available topical antifungal agents with regard to mycological cure, agents differ in their specific intrinsic properties, which can affect their clinical use. The addition of a corticosteroid to an antifungal agent at the initiation of treatment can attenuate the inflammatory symptoms of the infection and is thought to increase patient compliance, reduce the risk of bacterial superinfection and enhance the efficacy of the antifungal agent. However, incorrect use of antifungal-corticosteroid therapy may be associated with treatment failure and adverse effects. This review summarises available treatment options for superficial fungal infections and provides general treatment recommendations based on the consensus outcomes of an Expert Panel meeting on the topical treatment of superficial mycoses.
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http://dx.doi.org/10.1111/myc.12481DOI Listing
June 2016

Methuselah/Methuselah-like G protein-coupled receptors constitute an ancient metazoan gene family.

Sci Rep 2016 Feb 26;6:21801. Epub 2016 Feb 26.

Department of Biological Sciences, Wayne State University, 5047 Gullen Mall, Detroit, MI 48202.

Inconsistent conclusions have been drawn regarding the phylogenetic age of the Methuselah/Methuselah-like (Mth/Mthl) gene family of G protein-coupled receptors, the founding member of which regulates development and lifespan in Drosophila. Here we report the results from a targeted homolog search of 39 holozoan genomes and phylogenetic analysis of the conserved seven transmembrane domain. Our findings reveal that the Mth/Mthl gene family is ancient, has experienced numerous extinction and expansion events during metazoan evolution, and acquired the current definition of the Methuselah ectodomain during its exceptional expansion in arthropods. In addition, our findings identify Mthl1, Mthl5, Mthl14, and Mthl15 as the oldest Mth/Mthl gene family paralogs in Drosophila. Future studies of these genes have the potential to define ancestral functions of the Mth/Mthl gene family.
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http://dx.doi.org/10.1038/srep21801DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4768249PMC
February 2016

Unique features of a global human ectoparasite identified through sequencing of the bed bug genome.

Nat Commun 2016 Feb 2;7:10165. Epub 2016 Feb 2.

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas 77030, USA.

The bed bug, Cimex lectularius, has re-established itself as a ubiquitous human ectoparasite throughout much of the world during the past two decades. This global resurgence is likely linked to increased international travel and commerce in addition to widespread insecticide resistance. Analyses of the C. lectularius sequenced genome (650 Mb) and 14,220 predicted protein-coding genes provide a comprehensive representation of genes that are linked to traumatic insemination, a reduced chemosensory repertoire of genes related to obligate hematophagy, host-symbiont interactions, and several mechanisms of insecticide resistance. In addition, we document the presence of multiple putative lateral gene transfer events. Genome sequencing and annotation establish a solid foundation for future research on mechanisms of insecticide resistance, human-bed bug and symbiont-bed bug associations, and unique features of bed bug biology that contribute to the unprecedented success of C. lectularius as a human ectoparasite.
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http://dx.doi.org/10.1038/ncomms10165DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4740739PMC
February 2016

Interleukin-29 induces epithelial production of CXCR3A ligands and T-cell infiltration.

J Mol Med (Berl) 2016 Apr 26;94(4):391-400. Epub 2015 Nov 26.

Psoriasis Research and Treatment Center, University Hospital Charité, Berlin, Germany.

Unlabelled: Psoriasis is considered as a model for chronic immune-mediated disorders. Th17-cells are pivotal players in those diseases. Recently, we demonstrated that Th17-cells produce interleukin (IL)-29 and that IL-29 is highly present in psoriatic lesions. Whether IL-29, with its action on epithelial cells and melanocytes, contributes to psoriasis pathogenesis, was unknown so far. Analysis of IL-29-treated human keratinocytes revealed induction of the chemokines CXCL10, CXCL11, and, to a much lesser extent, CXCL9. Unlike these CXCR3A ligands, known to attract Th1-, CD8(+), NK-, and Th1/Th17 transient cells, no influence was found on chemokines attracting other immune cell populations or on molecules modulating the CXCR3A/CXCR3A ligand interaction. CXCR3A ligand expression was also induced by IL-29 in melanocytes and in epidermis models and explanted skin. Regarding other psoriasis-relevant cytokines, interferon-γ and, less potently, tumor necrosis factor-α and IL-1β shared and strengthened IL-29's capacity. Murine IL-29 counterpart injected into mouse skin provoked local CXCL10 and CXCL11 expression, T-cell infiltration, and, in consequence, skin swelling. The elevated IL-29 expression in psoriatic lesions was associated with upregulation of CXCR3A ligands compared to non-lesional skin of these patients and to the skin of healthy donors and atopic dermatitis patients, which lack IL-29 production. Importantly, neutralization of IL-29 reduced CXCR3A ligand levels in explant cultures of psoriatic lesions. Finally, elevated blood CXCL11 levels were found in psoriasis that might be useful for monitoring lesional activity of the IL-29 axis. In summary, the Th17-cytokine IL-29 induces specific chemokines and, in consequence, provokes skin infiltration of potentially pathogenic T-cells.

Key Messages: IL-29 selectively induces CXCR3A-binding chemokines (CXCL9, CXCL10, CXCL11) in skin cells. Murine IL-29 counterpart induces skin T-cell infiltration and inflammation in mice. CXCR3A ligands are IL-29-dependently increased in lesional skin of psoriasis patients. CXCR3A ligand levels in psoriatic skin correlate with epidermal T-cell numbers. Increased blood CXCL11 levels in psoriasis may be a biomarker for local IL-29 action.
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http://dx.doi.org/10.1007/s00109-015-1367-yDOI Listing
April 2016

Evo-Devo gene toolkit update: at least seven Pax transcription factor subfamilies in the last common ancestor of bilaterian animals.

Authors:
Markus Friedrich

Evol Dev 2015 Sep-Oct;17(5):255-7

Department of Biological Sciences, Wayne State University, 5047 Gullen Mall, Detroit, MI 48202, USA.

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http://dx.doi.org/10.1111/ede.12137DOI Listing
June 2016