Publications by authors named "Hidemasa Bono"

74 Publications

De novo transcriptome analysis for examination of the nutrition metabolic system related to the evolutionary process through which stick insects gain the ability of flight (Phasmatodea).

BMC Res Notes 2021 May 13;14(1):182. Epub 2021 May 13.

Database Center for Life Science (DBCLS), Joint Support-Center for Data Science Research, Research Organization of Information and Systems (ROIS), Mishima, Shizuoka, 411-8540, Japan.

Objective: Insects are the most evolutionarily successful groups of organisms, and this success is largely due to their flight ability. Interestingly, some stick insects have lost their flight ability despite having wings. To elucidate the shift from wingless to flying forms during insect evolution, we compared the nutritional metabolism system among flight-winged, flightless-winged, and flightless-wingless stick insect groups.

Results: Here, we report RNA sequencing of midgut transcriptome of Entoria okinawaensis, a prominent Japanese flightless-wingless stick insect, and the comparative analysis of its transcriptome in publicly available midgut transcriptomes obtained from seven stick insect species. A gene enrichment analysis for differentially expressed genes, including those obtained from winged vs wingless and flight vs flightless genes comparisons, revealed that carbohydrate metabolic process-related genes were highly expressed in the winged stick insect group. We also found that the expression of the mitochondrial enolase superfamily member 1 transcript was significantly higher in the winged stick insect group than in the wingless stick insect group. Our findings could indicate that carbohydrate metabolic processes are related to the evolutionary process through which stick insects gain the ability of flight.
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http://dx.doi.org/10.1186/s13104-021-05600-0DOI Listing
May 2021

Diversification of mineralocorticoid receptor genes in a subterranean rodent, the naked mole-rat.

J Mol Endocrinol 2021 May 11;66(4):299-311. Epub 2021 May 11.

Department of Aging and Longevity Research, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan.

Naked mole-rats (Heterocephalus glaber) inhabit subterranean burrows in savannas and are, thus, unable to access free water. To identify their mechanism of osmoregulation in xeric environments, we molecularly cloned and analyzed the nuclear receptor subfamily 3 group C member 2 (NR3C2) gene encoding the mineralocorticoid receptor (MR), required for hormone-dependent regulation of genes contributing to body fluid homeostasis. Most vertebrates harbor a single MR homolog. In contrast, we discovered that MR is duplicated in naked mole-rats. The amino acid sequence of naked mole-rat MR1 is 90% identical to its mouse ortholog, and MR1 is abundantly expressed in the kidney and the nervous system. MR2 encodes a truncated protein lacking DNA- and ligand-binding domains of MR1 and is expressed in diverse tissues. Although MR2 did not directly transactivate gene expression, it increased corticosteroid-dependent transcriptional activity of MR1. Our results suggest that MR2 might function as a novel regulator of MR1 activity to fine-tune MR signaling in naked mole-rats.
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http://dx.doi.org/10.1530/JME-20-0325DOI Listing
May 2021

Meta-Analysis of Oxidative Transcriptomes in Insects.

Authors:
Hidemasa Bono

Antioxidants (Basel) 2021 Feb 25;10(3). Epub 2021 Feb 25.

Program of Biomedical Science, Graduate School of Integrated Sciences for Life, Hiroshima University, 3-10-23 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-0046, Japan.

Data accumulation in public databases has resulted in extensive use of meta-analysis, a statistical analysis that combines the results of multiple studies. Oxidative stress occurs when there is an imbalance between free radical activity and antioxidant activity, which can be studied in insects by transcriptome analysis. This study aimed to apply a meta-analysis approach to evaluate insect oxidative transcriptomes using publicly available data. We collected oxidative stress response-related RNA sequencing (RNA-seq) data for a wide variety of insect species, mainly from public gene expression databases, by manual curation. Only RNA-seq data of were found and were systematically analyzed using a newly developed RNA-seq analysis workflow for species without a reference genome sequence. The results were evaluated by two metric methods to construct a reference dataset for oxidative stress response studies. Many genes were found to be downregulated under oxidative stress and related to organ system process (GO:0003008) and adherens junction organization (GO:0034332) by gene enrichment analysis. A cross-species analysis was also performed. RNA-seq data of were curated, since no RNA-seq data of insect species are currently available in public databases. This method, including the workflow developed, represents a powerful tool for deciphering conserved networks in oxidative stress response.
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http://dx.doi.org/10.3390/antiox10030345DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7996572PMC
February 2021

Full-length 16S rRNA gene amplicon analysis of human gut microbiota using MinION™ nanopore sequencing confers species-level resolution.

BMC Microbiol 2021 Jan 26;21(1):35. Epub 2021 Jan 26.

Department of Human Stress Response Science, Institute of Biomedical Science, Kansai Medical University, 2-5-1 Shin-machi, Hirakata, Osaka, 573-1010, Japan.

Background: Species-level genetic characterization of complex bacterial communities has important clinical applications in both diagnosis and treatment. Amplicon sequencing of the 16S ribosomal RNA (rRNA) gene has proven to be a powerful strategy for the taxonomic classification of bacteria. This study aims to improve the method for full-length 16S rRNA gene analysis using the nanopore long-read sequencer MinION™. We compared it to the conventional short-read sequencing method in both a mock bacterial community and human fecal samples.

Results: We modified our existing protocol for full-length 16S rRNA gene amplicon sequencing by MinION™. A new strategy for library construction with an optimized primer set overcame PCR-associated bias and enabled taxonomic classification across a broad range of bacterial species. We compared the performance of full-length and short-read 16S rRNA gene amplicon sequencing for the characterization of human gut microbiota with a complex bacterial composition. The relative abundance of dominant bacterial genera was highly similar between full-length and short-read sequencing. At the species level, MinION™ long-read sequencing had better resolution for discriminating between members of particular taxa such as Bifidobacterium, allowing an accurate representation of the sample bacterial composition.

Conclusions: Our present microbiome study, comparing the discriminatory power of full-length and short-read sequencing, clearly illustrated the analytical advantage of sequencing the full-length 16S rRNA gene.
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http://dx.doi.org/10.1186/s12866-021-02094-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7836573PMC
January 2021

Cigarette Smoke Extract Activates Hypoxia-Inducible Factors in a Reactive Oxygen Species-Dependent Manner in Stroma Cells from Human Endometrium.

Antioxidants (Basel) 2021 Jan 3;10(1). Epub 2021 Jan 3.

Department of Obstetrics and Gynecology, Kansai Medical University, 2-3-1 shinmachi-cho, Hirakata 573-1191, Japan.

Cigarette smoking (CS) is a major contributing factor in the development of a large number of fatal and debilitating disorders, including degenerative diseases and cancers. Smoking and passive smoking also affect the establishment and maintenance of pregnancy. However, to the best of our knowledge, the effects of smoking on the human endometrium remain poorly understood. In this study, we investigated the regulatory mechanism underlying CS-induced hypoxia-inducible factor (HIF)-1α activation using primary human endometrial stromal cells and an immortalized cell line (KC02-44D). We found that the CS extract (CSE) increased reactive oxygen species levels and stimulated HIF-1α protein stabilization in endometrial stromal cells, and that CS-induced HIF-1α-dependent gene expression under non-hypoxic conditions in a concentration- and time-dependent manner. Additionally, we revealed the upregulated expression of a hypoxia-induced gene set following the CSE treatment, even under normoxic conditions. These results indicated that HIF-1α might play an important role in CS-exposure-induced cellular stress, inflammation, and endometrial remodeling.
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http://dx.doi.org/10.3390/antiox10010048DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7823731PMC
January 2021

FANTOM enters 20th year: expansion of transcriptomic atlases and functional annotation of non-coding RNAs.

Nucleic Acids Res 2021 01;49(D1):D892-D898

RIKEN Center for Integrative Medical Sciences, Yokohama, Kanagawa, Japan.

The Functional ANnoTation Of the Mammalian genome (FANTOM) Consortium has continued to provide extensive resources in the pursuit of understanding the transcriptome, and transcriptional regulation, of mammalian genomes for the last 20 years. To share these resources with the research community, the FANTOM web-interfaces and databases are being regularly updated, enhanced and expanded with new data types. In recent years, the FANTOM Consortium's efforts have been mainly focused on creating new non-coding RNA datasets and resources. The existing FANTOM5 human and mouse miRNA atlas was supplemented with rat, dog, and chicken datasets. The sixth (latest) edition of the FANTOM project was launched to assess the function of human long non-coding RNAs (lncRNAs). From its creation until 2020, FANTOM6 has contributed to the research community a large dataset generated from the knock-down of 285 lncRNAs in human dermal fibroblasts; this is followed with extensive expression profiling and cellular phenotyping. Other updates to the FANTOM resource includes the reprocessing of the miRNA and promoter atlases of human, mouse and chicken with the latest reference genome assemblies. To facilitate the use and accessibility of all above resources we further enhanced FANTOM data viewers and web interfaces. The updated FANTOM web resource is publicly available at https://fantom.gsc.riken.jp/.
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http://dx.doi.org/10.1093/nar/gkaa1054DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7779024PMC
January 2021

Characterization of brown adipose tissue thermogenesis in the naked mole-rat (Heterocephalus glaber), a heterothermic mammal.

Sci Rep 2020 11 10;10(1):19488. Epub 2020 Nov 10.

Department of Aging and Longevity Research, Kumamoto University, Kumamoto, 860-0811, Japan.

The naked mole-rat (NMR) is a heterothermic mammal that forms eusocial colonies consisting of one reproductive female (queen), several reproductive males, and subordinates. Despite their heterothermy, NMRs possess brown adipose tissue (BAT), which generally induces thermogenesis in cold and some non-cold environments. Previous studies suggest that NMR-BAT induces thermogenesis by cold exposure. However, detailed NMR-BAT characteristics and whether NMR-BAT thermogenesis occurs in non-cold environments are unknown. Here, we show beta-3 adrenergic receptor (ADRB3)-dependent thermogenic potential of NMR-BAT, which contributes to thermogenesis in the isolated queen in non-cold environments (30 °C). NMR-BAT expressed several brown adipocyte marker genes and showed noradrenaline-dependent thermogenic activity in vitro and in vivo. Although our ADRB3 inhibition experiments revealed that NMR-BAT thermogenesis slightly delays the decrease in body temperature in a cold environment (20 °C), it was insufficient to prevent the decrease in the body temperatures. Even at 30 °C, NMRs are known to prevent the decrease of and maintain their body temperature by heat-sharing behaviors within the colony. However, isolated NMRs maintained their body temperature at the same level as when they are in the colony. Interestingly, we found that queens, but not subordinates, induce BAT thermogenesis in this condition. Our research provides novel insights into NMR thermoregulation.
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http://dx.doi.org/10.1038/s41598-020-74929-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7656259PMC
November 2020

Construction of TUATinsecta database that integrated plant and insect database for screening phytophagous insect metabolic products with medicinal potential.

Sci Rep 2020 10 15;10(1):17509. Epub 2020 Oct 15.

Department of Science of Biological Production, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu-shi, Tokyo, 183-8509, Japan.

Phytophagous insect larvae feed on plants containing secondary metabolic products with biological activity against other predatory organisms. Phytophagous insects can use their specialised metabolic systems to covert these secondary metabolic products into compounds with therapeutic properties useful to mankind. Some Asians drink tea decoctions made from phytophagous insect frass which is believed to be effective against inflammatory diseases. However, insects that can convert plant-derived secondary metabolic products into useful human therapeutic agents remain poorly studied. Here, we constructed the TUATinsecta database by integrating publicly plant/insect datasets for the purpose of selecting insect species. Using TUAT-insecta we selected the Asian swallowtail butterfly, Papilio xuthus larvae fed on several species of Rutaceous plants and examined whether the plant-derived secondary metabolites, especially those present in frass, were chemically altered or not. We extracted metabolic products from frass using three organic solvents with different polarities, and evaluated solvent fractions for their cytotoxic effects against several human cell lines. We found that chloroform frass extracts from P. xuthus larvae fed on Poncirus trifoliata leaves contained significant cytotoxic activity. Our findings demonstrate that screening of insect species using the 'TUATinsecta' database provides an important pipeline for discovering novel therapeutic agents that might be useful for mankind.
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http://dx.doi.org/10.1038/s41598-020-74590-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7566601PMC
October 2020

Functional annotation of human long noncoding RNAs via molecular phenotyping.

Genome Res 2020 07 27;30(7):1060-1072. Epub 2020 Jul 27.

Department of Computational Systems Biology, Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow 119991, Russia.

Long noncoding RNAs (lncRNAs) constitute the majority of transcripts in the mammalian genomes, and yet, their functions remain largely unknown. As part of the FANTOM6 project, we systematically knocked down the expression of 285 lncRNAs in human dermal fibroblasts and quantified cellular growth, morphological changes, and transcriptomic responses using Capped Analysis of Gene Expression (CAGE). Antisense oligonucleotides targeting the same lncRNAs exhibited global concordance, and the molecular phenotype, measured by CAGE, recapitulated the observed cellular phenotypes while providing additional insights on the affected genes and pathways. Here, we disseminate the largest-to-date lncRNA knockdown data set with molecular phenotyping (over 1000 CAGE deep-sequencing libraries) for further exploration and highlight functional roles for and .
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http://dx.doi.org/10.1101/gr.254219.119DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7397864PMC
July 2020

BioHackathon 2015: Semantics of data for life sciences and reproducible research.

F1000Res 2020 24;9:136. Epub 2020 Feb 24.

St Vincent's Clinical School, Faculty of Medicine, University of New South Wales, Darlinghurst, Australia.

We report on the activities of the 2015 edition of the BioHackathon, an annual event that brings together researchers and developers from around the world to develop tools and technologies that promote the reusability of biological data. We discuss issues surrounding the representation, publication, integration, mining and reuse of biological data and metadata across a wide range of biomedical data types of relevance for the life sciences, including chemistry, genotypes and phenotypes, orthology and phylogeny, proteomics, genomics, glycomics, and metabolomics. We describe our progress to address ongoing challenges to the reusability and reproducibility of research results, and identify outstanding issues that continue to impede the progress of bioinformatics research. We share our perspective on the state of the art, continued challenges, and goals for future research and development for the life sciences Semantic Web.
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http://dx.doi.org/10.12688/f1000research.18236.1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7141167PMC
February 2021

Thyroid Hormone Facilitates in vitro Decidualization of Human Endometrial Stromal Cells via Thyroid Hormone Receptors.

Endocrinology 2020 06;161(6)

Department of Obstetrics and Gynecology, Kansai Medical University, Hirakata, Japan.

Endometrial stromal cells differentiate into decidual cells through the process of decidualization. This differentiation is critical for embryo implantation and the successful establishment of pregnancy. Recent epidemiological studies have suggested that thyroid hormone is important in the endometrium during implantation, and it is commonly believed that thyroid hormone is essential for proper development, differentiation, growth, and metabolism. This study aimed to investigate the impact of thyroid hormone on decidualization in human endometrial stromal cells (hESCs) and define its physiological roles in vitro by gene targeting. To identify the expression patterns of thyroid hormone, we performed gene expression profiling of hESCs during decidualization after treating them with the thyroid hormone levothyroxine (LT4). A major increase in decidual response was observed after combined treatment with ovarian steroid hormones and thyroid hormone. Moreover, LT4 treatment also affected the regulation of many transcription factors important for decidualization. We found that type 3 deiodinase, which is particularly important in fetal and placental tissues, was upregulated during decidualization in the presence of thyroid hormone. Further, it was observed that progesterone receptor, an ovarian steroid hormone receptor, was involved in thyroid hormone-induced decidualization. In the absence of thyroid hormone receptor (TR), due to the simultaneous silencing of TRα and TRβ, thyroid hormone expression was unchanged during decidualization. In summary, we demonstrated that thyroid hormone is essential for decidualization in the endometrium. This is the first in vitro study to find impaired decidualization as a possible cause of infertility in subclinical hypothyroidism (SCH) patients.
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http://dx.doi.org/10.1210/endocr/bqaa049DOI Listing
June 2020

GLIS1, a novel hypoxia-inducible transcription factor, promotes breast cancer cell motility via activation of WNT5A.

Carcinogenesis 2020 09;41(9):1184-1194

Department of Radiation Disaster Medicine, Research Institute for Radiation Biology and Medicine, Hiroshima University, Hiroshima, Japan.

We previously demonstrated that expression of a Krüppel-like zinc finger transcription factor, GLIS1, dramatically increases under hypoxic conditions via a transcriptional mechanism induced by HIF-2α cooperating with AP-1 members. In this study, we focused on the functional roles of GLIS1 in breast cancer. To uncover its biological function, the effects of altered levels of GLIS1 in breast cancer cell lines on cellular growth, wound-healing and invasion capacities were assessed. Knockdown of GLIS1 using siRNA in BT-474 cells resulted in significant growth stimulation under normoxia, while attenuation was found in the cell invasion assay under hypoxic conditions. In MDA-MB-231 cells expressing exogenous 3xFLAG-tagged GLIS1, GLIS1 attenuated cell proliferation and enhanced cell mobility and invasion capacities under normoxia. In addition, breast cancer cells expressing GLIS1 acquired resistance to irradiation. Whole transcriptome analysis clearly demonstrated that downstream signals of GLIS1 are related to various cellular functions. Among the genes with increased expression, we focused on WNT5A. Knockdown of WNT5A indicated that enhancement of acquired cell motility in the MDA-MB-231 cells expressing GLIS1 was mediated, at least in part, by WNT5A. In an analysis of publicly available data, patients with estrogen receptor-negative breast cancer showing high levels of GLIS1 expression showed much worse prognosis than those with low levels. In summary, hypoxia-induced GLIS1 plays significant roles in breast cancer cells via regulation of gene expression related to cell migration and invasion capacities, resulting in poorer prognosis in patients with advanced breast cancer.
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http://dx.doi.org/10.1093/carcin/bgaa010DOI Listing
September 2020

Analysis of molecular mechanism for acceleration of polyembryony using gene functional annotation pipeline in Copidosoma floridanum.

BMC Genomics 2020 Feb 11;21(1):152. Epub 2020 Feb 11.

Department of Science of Biological Production, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Tokyo, Japan.

Background: Polyembryony is defined as the formation of several embryos from a single egg. This phenomenon can occur in humans, armadillo, and some endoparasitoid insects. However, the mechanism underlying polyembryogenesis in animals remains to be elucidated. The polyembryonic parasitoid wasp Copidosoma floridanum oviposits its egg into an egg of the host insect; eventually, over 2000 individuals will arise from one egg. Previously, we reported that polyembryogenesis is enhanced when the juvenile hormone (JH) added to the culture medium in the embryo culture. Hence, in the present study, we performed RNA sequencing (RNA-Seq) analysis to investigate the molecular mechanisms controlling polyembryogenesis of C. floridanum. Functional annotation of genes is not fully available for C.floridanum; however, whole genome assembly has been archived. Hence, we constructed a pipeline for gene functional annotation in C. floridanum and performed molecular network analysis. We analyzed differentially expressed genes between control and JH-treated molura after 48 h of culture, then used the tblastx program to assign whole C. floridanum transcripts to human gene.

Results: We obtained 11,117 transcripts in the JH treatment group and identified 217 differentially expressed genes compared with the control group. As a result, 76% of C. floridanum transcripts were assigned to human genes. Gene enrichment analysis revealed genes associated with platelet degranulation, fatty acid biosynthesis, cell morphogenesis in the differentiation and integrin signaling pathways were fluctuated following JH treatment. Furthermore, Cytoscape analysis revealed a molecular interaction that was possibly associated with polyembryogenesis .

Conclusions: We have constructed a pipeline for gene functional annotation of C. floridanum, and identified transcripts with high similarity to human genes during early embryo developmental. Additionally, this study reveals new molecular interactions associated with polyembryogenesis; these interactions could indicate the molecular mechanisms underlying polyembryony. Our results highlight the potential utility of molecular interaction analysis in human twins.
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http://dx.doi.org/10.1186/s12864-020-6559-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7014612PMC
February 2020

All of gene expression (AOE): An integrated index for public gene expression databases.

Authors:
Hidemasa Bono

PLoS One 2020 24;15(1):e0227076. Epub 2020 Jan 24.

Database Center for Life Science (DBCLS), Joint Support-Center for Data Science Research, Research Organization of Information and Systems, Mishima,Japan.

Gene expression data have been archived as microarray and RNA-seq datasets in two public databases, Gene Expression Omnibus (GEO) and ArrayExpress (AE). In 2018, the DNA DataBank of Japan started a similar repository called the Genomic Expression Archive (GEA). These databases are useful resources for the functional interpretation of genes, but have been separately maintained and may lack RNA-seq data, while the original sequence data are available in the Sequence Read Archive (SRA). We constructed an index for those gene expression data repositories, called All Of gene Expression (AOE), to integrate publicly available gene expression data. The web interface of AOE can graphically query data in addition to the application programming interface. By collecting gene expression data from RNA-seq in the SRA, AOE also includes data not included in GEO and AE. AOE is accessible as a search tool from the GEA website and is freely available at https://aoe.dbcls.jp/.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0227076PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6980531PMC
April 2020

Meta-Analysis of Hypoxic Transcriptomes from Public Databases.

Biomedicines 2020 Jan 9;8(1). Epub 2020 Jan 9.

Department of Human Stress Response Science, Institute of Biomedical Science, Kansai Medical University, Hirakata 573-1010, Japan.

Hypoxia is the insufficiency of oxygen in the cell, and hypoxia-inducible factors (HIFs) are central regulators of oxygen homeostasis. In order to obtain functional insights into the hypoxic response in a data-driven way, we attempted a meta-analysis of the RNA-seq data from the hypoxic transcriptomes archived in public databases. In view of methodological variability of archived data in the databases, we first manually curated RNA-seq data from appropriate pairs of transcriptomes before and after hypoxic stress. These included 128 human and 52 murine transcriptome pairs. We classified the results of experiments for each gene into three categories: upregulated, downregulated, and unchanged. Hypoxic transcriptomes were then compared between humans and mice to identify common hypoxia-responsive genes. In addition, meta-analyzed hypoxic transcriptome data were integrated with public ChIP-seq data on the known human HIFs, HIF-1 and HIF-2, to provide insights into hypoxia-responsive pathways involving direct transcription factor binding. This study provides a useful resource for hypoxia research. It also demonstrates the potential of a meta-analysis approach to public gene expression databases for selecting candidate genes from gene expression profiles generated under various experimental conditions.
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http://dx.doi.org/10.3390/biomedicines8010010DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7168238PMC
January 2020

Superoxide dismutase down-regulation and the oxidative stress is required to initiate pupation in Bombyx mori.

Sci Rep 2019 10 11;9(1):14693. Epub 2019 Oct 11.

Department of United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo, 183-8509, Japan.

Perhaps, oxidative stress progresses pupation in some Lepidopteran insects; however, the reasons for this remain obscure. In our previous study, we clarified Bombyx mori SOD1 (BmSOD1) and B. mori SOD2 (BmSOD2) proteins respond in common to ultraviolet irradiation (UV) oxidative stress and metamorphosis. This result strongly suggested pupation initiates by oxidative stress and might mediate by down-regulation of expression of BmSOD1 and BmSOD2 proteins. Thus, we examined about these relationships in B. mori in this study. In the microarray data reanalysis, we found the Notch signaling pathways as the common pathways in pupation and UV oxidative stress in B. mori. Also, we showed a molting hormone, 20-hydroxyecdysone, leads not only generation of superoxide but also downregulation of the expression of BmSOD proteins during pupation in B. mori. Our findings can contribute to a deeper understanding of how biological defense systems work against environmental oxidative stress.
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http://dx.doi.org/10.1038/s41598-019-51163-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6788986PMC
October 2019

Apoptosis-mediated vasa down-regulation controls developmental transformation in Japanese Copidosoma floridanum female soldiers.

Dev Biol 2019 12 19;456(2):226-233. Epub 2019 Sep 19.

Department of Science of Biological Production, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo, 183-8509, Japan. Electronic address:

Copidosoma floridanum is a polyembryonic, caste-forming, wasp species. The ratio of investment in different castes changes with environmental stressors (e.g. multi-parasitism with competitors). The vasa gene was first identified in Drosophila melanogaster as a germ-cell-determining factor, and C. floridanum vasa (Cf-vas) gene positive cells have been known to develop into reproductive larvae. Cf-vas seems to control the ratio of investment in C. floridanum larval castes. In this study, we identified environmental factors that control Cf-vas mRNA expression in Japanese C. floridanum by examining Cf-vas mRNA expression under competitor (Meteorus pulchricornis) venom stress; we treated the male and female morulae with M. pulchricornis venom. We also assessed the effects of multi-parasitism of Japanese C. floridanum with M. pulchricornis and found an increasing number of female soldier larvae. The results showed that several amino acid sequences differ between the Japanese and US Cf-vas. Quantitative reverse transcription polymerase chain reaction (qRT-PCR) showed that Japanese Cf-vas mRNA is expressed in both male and female larvae and pupae, but mRNA expression decreases in adults. Cf-vas mRNA expression significantly decreased, while C. floridanum dronc (Cf-dronc) mRNA expression increased, in female morulae after M. pulchricornis venom treatment at 20 h and 0 h of the culture period, respectively. Females and males showed different Cf-vas or Cf-dronc mRNA expression after M. pulchricornis venom treatment. Therefore, M. pulchricornis venom could affect the ratio of investment in different female castes of Japanese C. floridanum by decreasing Cf-vas mRNA expression via apoptosis.
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http://dx.doi.org/10.1016/j.ydbio.2019.09.005DOI Listing
December 2019

Cancerous phenotypes associated with hypoxia-inducible factors are not influenced by the volatile anesthetic isoflurane in renal cell carcinoma.

PLoS One 2019 15;14(4):e0215072. Epub 2019 Apr 15.

Department of Human Stress Response Science, Institute of Biomedical Science, Kansai Medical University, Hirakata, Japan.

The possibility that anesthesia during cancer surgery may affect cancer recurrence, metastasis, and patient prognosis has become one of the most important topics of interest in cancer treatment. For example, the volatile anesthetic isoflurane was reported in several studies to induce hypoxia-inducible factors, and thereby enhance malignant phenotypes in vitro. Indeed, these transcription factors are considered critical regulators of cancer-related hallmarks, including "sustained proliferative signaling, evasion of growth suppressors, resistance to cell death, replicative immortality, angiogenesis, invasion, and metastasis." This study aimed to investigate the impact of isoflurane on the growth and migration of derivatives of the renal cell line RCC4. We indicated that isoflurane treatment did not positively influence cancer cell phenotypes, and that hypoxia-inducible factors (HIFs) maintain hallmark cancer cell phenotypes including gene expressions signature, metabolism, cell proliferation and cell motility. The present results indicate that HIF activity is not influenced by the volatile anesthetic isoflurane.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0215072PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6464189PMC
January 2020

Comparative analysis of seven types of superoxide dismutases for their ability to respond to oxidative stress in Bombyx mori.

Sci Rep 2019 02 18;9(1):2170. Epub 2019 Feb 18.

Department of Science of Biological Production, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo, 183-8509, Japan.

Insects are well adapted to changing environmental conditions. They have unique systems for eliminating reactive oxygen species (ROS). Superoxide dismutase (SOD) is a key enzyme that plays a primary role in removing ROS. Bombyx mori is a lepidopteran insect, whose body size is larger than the model insect Drosophila melanogaster, which enabled us to more easily examine gene expression at the tissue level. We searched B. mori SOD (BmSOD) genes using genome database, and we analyzed their function under different type of oxidative stress. Consequently, we identified four new types of BmSODs in addition to the three types already known. Two of the seven types had a unique domain architecture that has not been discovered previously in the SOD family, and they were expressed in different tissues and developmental stages. Furthermore, these BmSODs responded differently to several kinds of stressors. Our results showed that the seven types of BmSODs are likely to play different roles in B. mori; therefore, B. mori could be used to distinguish the functions of each SOD for resistance to oxidative stress that changes with the environmental conditions.
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http://dx.doi.org/10.1038/s41598-018-38384-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6379424PMC
February 2019

Suppression of mitochondrial oxygen metabolism mediated by the transcription factor HIF-1 alleviates propofol-induced cell toxicity.

Sci Rep 2018 06 12;8(1):8987. Epub 2018 Jun 12.

Department of Human Stress Response Science, Institute of Biomedical Science, Kansai Medical University, Hirakata, Japan.

A line of studies strongly suggest that the intravenous anesthetic, propofol, suppresses mitochondrial oxygen metabolism. It is also indicated that propofol induces the cell death in a reactive oxygen species (ROS)-dependent manner. Because hypoxia-inducible factor 1 (HIF-1) is a transcription factor which is involved in cellular metabolic reprogramming by modulating gene expressions of enzymes including glycolysis pathway and oxygen utilization of mitochondria, we examined the functional role of HIF-1 activity in propofol-induced cell death. The role of HIF-1 activity on oxygen and energy metabolisms and propofol-induced cell death and caspase activity was examined in renal cell-derived RCC4 cells: RCC4-EV cells which lack von Hippel-Lindau protein (VHL) protein expression and RCC4-VHL cells, which express exogenous VHL, and in neuronal SH-SY5Y cells. It was demonstrated that HIF-1 is involved in suppressing oxygen consumption and facilitating glycolysis in cells and that the resistance to propofol-induced cell death was established in a HIF-1 activation-dependent manner. It was also demonstrated that HIF-1 activation by treatment with HIFα-hydroxylase inhibitors such as n-propyl gallate and dimethyloxaloylglycine, alleviated the toxic effects of propofol. Thus, the resistance to propofol toxicity was conferred by HIF-1 activation by not only genetic deletion of VHL but also exposure to HIFα-hydroxylase inhibitors.
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http://dx.doi.org/10.1038/s41598-018-27220-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5997661PMC
June 2018

Promotion of malignant phenotype after disruption of the three-dimensional structure of cultured spheroids from colorectal cancer.

Oncotarget 2018 Mar 23;9(22):15968-15983. Epub 2018 Mar 23.

Department of Biochemistry, Osaka International Cancer Institute, Chuo-ku, Osaka, Japan.

Individual and small clusters of cancer cells may detach from the edges of a main tumor and invade vessels, which can act as the origin of metastasis; however, the mechanism for this phenomenon is not well understood. Using cancer tissue-originated spheroids, we studied whether disturbing the 3D architecture of cancer spheroids can provoke the reformation process and progression of malignancy. We developed a mechanical disruption method to achieve homogenous disruption of the spheroids while maintaining cell-cell contact. After the disruption, 9 spheroid lines from 9 patient samples reformed within a few hours, and 3 of the 9 lines exhibited accelerated spheroid growth. Marker expression, spheroid forming capacity, and tumorigenesis indicated that stemness increased after spheroid disruption. In addition, the spheroid forming capacity increased in 6 of 11 spheroid lines. The disruption signature determined by gene expression profiling supported the incidence of remodeling and predicted the prognosis of patients with colorectal cancer. Furthermore, WNT and HER3 signaling were increased in the reformed spheroids, and suppression of these signaling pathways attenuated the increased proliferation and stemness after the disruption. Overall, the disruption and subsequent reformation of cancer spheroids promoted malignancy-related phenotypes through the activation of the WNT and ERBB pathways.
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http://dx.doi.org/10.18632/oncotarget.24641DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5882311PMC
March 2018

Construction of a simple evaluation system for the intestinal absorption of an orally administered medicine using Bombyx mori larvae.

Drug Discov Ther 2018;12(1):7-15

Department of Science of Biological Production, Graduate School of Agriculture, Tokyo University of Agriculture and Technology.

Human intestinal absorption is estimated using a human colon carcinoma cell line (Caco-2) cells from human colorectal adenocarcinoma, intestinal perfusion, or a mammalian model. These current evaluation systems are limited in their ability to estimate human intestinal absorption. In addition, in vivo evaluation systems using laboratory animals such as mice and rats entail animal ethics problems, and it is difficult to screen compounds on a large scale at the drug discovery stage. Thus, we propose the use of Bombyx mori larvae for evaluation of intestinal absorption of compounds as an alternative system in this study. First, to compare the characteristics among Caco-2 cells, human intestine, and B. mori larval midgut, we analyzed their RNA-seq data, and we found 26 drug transporters common to humans and B. mori. Next, we quantitatively developed an oral administration technique in B. mori and established a method using silkworm B. mori larvae that can easily estimate the intestinal permeability of compounds. Consequently, we could determine the dose and technique for oral administration in B. mori larvae. We also developed a B. mori model to evaluate the intestinal permeability of orally administered. Our constructed evaluation system will be useful for evaluating intestinal permeability in medical drug development.
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http://dx.doi.org/10.5582/ddt.2018.01004DOI Listing
August 2019

Differentiated embryo chondrocyte plays a crucial role in DNA damage response via transcriptional regulation under hypoxic conditions.

PLoS One 2018 21;13(2):e0192136. Epub 2018 Feb 21.

Department of Radiation Medicine, Research Institute for Radiation Biology and Medicine, Hiroshima University, Hiroshima, Japan.

Tumor hypoxia contributes to a biologically aggressive phenotype and therapeutic resistance. Recent studies have revealed that hypoxia reduces expression of several DNA damage recognition and repair (DRR) genes via both hypoxia-inducible factor (HIF)-independent and -dependent pathways, and this induced genomic instability in cancer cells. We show here that one of the HIF-target genes-differentiated embryo chondrocyte (DEC)-plays a role in DNA damage response via transcriptional repression. Comprehensive gene expression and database analyses have revealed systemic repression of DNA-DRR genes in cancer and non-cancer cells under hypoxic conditions. Hypoxic repression in typical cases was confirmed by quantitative RT-PCR and promoter reporter experiments, and knockdown experiments indicated the critical role of DEC2 in such repression. Assessment of histone H2AX phosphorylation revealed that recognition and repair of DNA double-strand breaks (DSBs) induced by bleomycin or γ-ray irradiation were attenuated; moreover, Cleaved Caspase-3 levels were decreased with pre-conditioning under hypoxia: opposing phenomena were ascertained by knockdown of DEC2. Finally, pre-conditioning under hypoxia decreased the sensitivity of cancer cells to DSBs, and knockdown of DEC2 increased γ-ray sensitivity. These data imply that a critical reduction of DNA-DRR occurs via DEC-dependent transcriptional repression and suggest that DEC is a potential molecular target for anti-cancer strategies.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0192136PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5821451PMC
March 2018

RefEx, a reference gene expression dataset as a web tool for the functional analysis of genes.

Sci Data 2017 08 29;4:170105. Epub 2017 Aug 29.

Database Center for Life Science, Joint Support-Center for Data Science Research, Research Organization of Information and Systems, 1111 Yata, Mishima 411-8540, Japan.

Gene expression data are exponentially accumulating; thus, the functional annotation of such sequence data from metadata is urgently required. However, life scientists have difficulty utilizing the available data due to its sheer magnitude and complicated access. We have developed a web tool for browsing reference gene expression pattern of mammalian tissues and cell lines measured using different methods, which should facilitate the reuse of the precious data archived in several public databases. The web tool is called Reference Expression dataset (RefEx), and RefEx allows users to search by the gene name, various types of IDs, chromosomal regions in genetic maps, gene family based on InterPro, gene expression patterns, or biological categories based on Gene Ontology. RefEx also provides information about genes with tissue-specific expression, and the relative gene expression values are shown as choropleth maps on 3D human body images from BodyParts3D. Combined with the newly incorporated Functional Annotation of Mammals (FANTOM) dataset, RefEx provides insight regarding the functional interpretation of unfamiliar genes. RefEx is publicly available at http://refex.dbcls.jp/.
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http://dx.doi.org/10.1038/sdata.2017.105DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5574374PMC
August 2017

HIF-1-mediated suppression of mitochondria electron transport chain function confers resistance to lidocaine-induced cell death.

Sci Rep 2017 06 19;7(1):3816. Epub 2017 Jun 19.

Department of Human Stress Response Science, Institute of Biomedical Science, Kansai Medical University, Hirakata, Japan.

The local anesthetic lidocaine induces cell death by altering reactive oxygen species (ROS) generation and mitochondrial electron transport chain function. Because hypoxia-inducible factor 1 (HIF-1) is involved in determining oxygen metabolism and mitochondria function, we investigated the involvement of HIF-1 activity in lidocaine-induced cell death. We investigated the role of HIF activation on lidocaine-induced caspase activation and cell death in renal cell-derived RCC4 cells lacking functional von Hippel-Lindau (VHL) protein. We demonstrate that HIF-1 suppressed oxygen consumption and facilitated glycolysis in a pyruvate dehydrogenase kinase-1-dependent manner and that activation of HIF-1 conferred resistance to lidocaine-induced cell death. We also demonstrated that exogenous HIF-1 activation, through HIFα-hydroxylase inhibition or exposure to hypoxic conditions, alleviates lidocaine toxicity by suppressing mitochondria function and generating ROS, not only in RCC4 cells, but also in the neuronal SH-SY5Y cells. In conclusion, we demonstrate that HIF-1 activation due to VHL deletion, treatment with small molecule HIFα-hydroxylase inhibitors, and exposure to hypoxic conditions suppresses mitochondrial respiratory chain function and confers resistance to lidocaine toxicity.
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http://dx.doi.org/10.1038/s41598-017-03980-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5476559PMC
June 2017

Calculating the quality of public high-throughput sequencing data to obtain a suitable subset for reanalysis from the Sequence Read Archive.

Gigascience 2017 06;6(6):1-8

It is important for public data repositories to promote the reuse of archived data. In the growing field of omics science, however, the increasing number of submissions of high-throughput sequencing (HTSeq) data to public repositories prevents users from choosing a suitable data set from among the large number of search results. Repository users need to be able to set a threshold to reduce the number of results to obtain a suitable subset of high-quality data for reanalysis. We calculated the quality of sequencing data archived in a public data repository, the Sequence Read Archive (SRA), by using the quality control software FastQC. We obtained quality values for 1 171 313 experiments, which can be used to evaluate the suitability of data for reuse. We also visualized the data distribution in SRA by integrating the quality information and metadata of experiments and samples. We provide quality information of all of the archived sequencing data, which enable users to obtain sufficient quality sequencing data for reanalyses. The calculated quality data are available to the public in various formats. Our data also provide an example of enhancing the reuse of public data by adding metadata to published research data by a third party.
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http://dx.doi.org/10.1093/gigascience/gix029DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5459929PMC
June 2017

Identification of functional enolase genes of the silkworm Bombyx mori from public databases with a combination of dry and wet bench processes.

BMC Genomics 2017 01 13;18(1):83. Epub 2017 Jan 13.

Department of Science of Biological Production, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo, 183-8509, Japan.

Background: Various insect species have been added to genomic databases over the years. Thus, researchers can easily obtain online genomic information on invertebrates and insects. However, many incorrectly annotated genes are included in these databases, which can prevent the correct interpretation of subsequent functional analyses. To address this problem, we used a combination of dry and wet bench processes to select functional genes from public databases.

Results: Enolase is an important glycolytic enzyme in all organisms. We used a combination of dry and wet bench processes to identify functional enolases in the silkworm Bombyx mori (BmEno). First, we detected five annotated enolases from public databases using a Hidden Markov Model (HMM) search, and then through cDNA cloning, Northern blotting, and RNA-seq analysis, we revealed three functional enolases in B. mori: BmEno1, BmEno2, and BmEnoC. BmEno1 contained a conserved key amino acid residue for metal binding and substrate binding in other species. However, BmEno2 and BmEnoC showed a change in this key amino acid. Phylogenetic analysis showed that BmEno2 and BmEnoC were distinct from BmEno1 and other enolases, and were distributed only in lepidopteran clusters. BmEno1 was expressed in all of the tissues used in our study. In contrast, BmEno2 was mainly expressed in the testis with some expression in the ovary and suboesophageal ganglion. BmEnoC was weakly expressed in the testis. Quantitative RT-PCR showed that the mRNA expression of BmEno2 and BmEnoC correlated with testis development; thus, BmEno2 and BmEnoC may be related to lepidopteran-specific spermiogenesis.

Conclusions: We identified and characterized three functional enolases from public databases with a combination of dry and wet bench processes in the silkworm B. mori. In addition, we determined that BmEno2 and BmEnoC had species-specific functions. Our strategy could be helpful for the detection of minor genes and functional genes in non-model organisms from public databases.
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http://dx.doi.org/10.1186/s12864-016-3455-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5237310PMC
January 2017

Update of the FANTOM web resource: high resolution transcriptome of diverse cell types in mammals.

Nucleic Acids Res 2017 01 27;45(D1):D737-D743. Epub 2016 Oct 27.

Division of Genomic Technologies (DGT), RIKEN Center for Life Science Technologie, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan

Upon the first publication of the fifth iteration of the Functional Annotation of Mammalian Genomes collaborative project, FANTOM5, we gathered a series of primary data and database systems into the FANTOM web resource (http://fantom.gsc.riken.jp) to facilitate researchers to explore transcriptional regulation and cellular states. In the course of the collaboration, primary data and analysis results have been expanded, and functionalities of the database systems enhanced. We believe that our data and web systems are invaluable resources, and we think the scientific community will benefit for this recent update to deepen their understanding of mammalian cellular organization. We introduce the contents of FANTOM5 here, report recent updates in the web resource and provide future perspectives.
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http://dx.doi.org/10.1093/nar/gkw995DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5210666PMC
January 2017

Tumour resistance in induced pluripotent stem cells derived from naked mole-rats.

Nat Commun 2016 05 10;7:11471. Epub 2016 May 10.

Biomedical Animal Research Laboratory, Institute for Genetic Medicine, Hokkaido University, Hokkaido 060-0815, Japan.

The naked mole-rat (NMR, Heterocephalus glaber), which is the longest-lived rodent species, exhibits extraordinary resistance to cancer. Here we report that NMR somatic cells exhibit a unique tumour-suppressor response to reprogramming induction. In this study, we generate NMR-induced pluripotent stem cells (NMR-iPSCs) and find that NMR-iPSCs do not exhibit teratoma-forming tumorigenicity due to the species-specific activation of tumour-suppressor alternative reading frame (ARF) and a disruption mutation of the oncogene ES cell-expressed Ras (ERAS). The forced expression of Arf in mouse iPSCs markedly reduces tumorigenicity. Furthermore, we identify an NMR-specific tumour-suppression phenotype-ARF suppression-induced senescence (ASIS)-that may protect iPSCs and somatic cells from ARF suppression and, as a consequence, tumorigenicity. Thus, NMR-specific ARF regulation and the disruption of ERAS regulate tumour resistance in NMR-iPSCs. Our findings obtained from studies of NMR-iPSCs provide new insight into the mechanisms of tumorigenicity in iPSCs and cancer resistance in the NMR.
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http://dx.doi.org/10.1038/ncomms11471DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4866046PMC
May 2016