Papers - Kanai, Akio

Editorial: Current Advances in the Research of RNA Regulatory Enzymes

Kanai, A. and Yoshihisa, T.

Frontiers in Genetics (Frontiers)  10 ( 973 )  2019.10

Research paper (scientific journal), Joint Work, Accepted

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Large-scale Molecular Evolutionary Analysis Uncovers a Variety of Polynucleotide Kinase Clp1 Family Proteins in the Three Domains of Life

Saito, M., Sato, A., Nagata, S., Tamaki, S., Tomita, M., Suzuki, H., and Kanai, A.

Genome Biology and Evolution (Genome Biology and Evolution)  11 ( 10 ) 2713 - 2726 2019.09

Research paper (scientific journal), Last author, Corresponding author, Accepted

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© 2019 The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. Clp1, a polyribonucleotide 5′-hydroxyl kinase in eukaryotes, is involved in pretRNA splicing and mRNA 3′-end formation. Enzymes similar in amino acid sequence to Clp1, Nol9, and Grc3, are present in some eukaryotes and are involved in prerRNA processing. However, our knowledge of how these Clp1 family proteins evolved and diversified is limited. We conducted a large-scale molecular evolutionary analysis of the Clp1 family proteins in all living organisms for which protein sequences are available in public databases. The phylogenetic distribution and frequencies of the Clp1 family proteins were investigated in complete genomes of Bacteria, Archaea and Eukarya. In total, 3,557 Clp1 family proteins were detected in the three domains of life, Bacteria, Archaea, and Eukarya. Many were from Archaea and Eukarya, but a few were found in restricted, phylogenetically diverse bacterial species. The domain structures of the Clp1 family proteins also differed among the three domains of life. Although the proteins were, on average, 555 amino acids long (range, 196-2,728), 122 large proteins with >1,000 amino acids were detected in eukaryotes. These novel proteins contain the conserved Clp1 polynucleotide kinase domain and various other functional domains. Of these proteins, >80% were from Fungi or Protostomia. The polyribonucleotide kinase activity of Thermus scotoductus Clp1 (Ts-Clp1) was characterized experimentally. Ts-Clp1 preferentially phosphorylates single-stranded RNA oligonucleotides (Km value for ATP, 2.5 μM), or single-stranded DNA at higher enzyme concentrations. We propose a comprehensive assessment of the diversification of the Clp1 family proteins and the molecular evolution of their functional domains.

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Systematic analysis of the binding surfaces between tRNAs and their respective aminoacyl tRNA synthetase based on structural and evolutionary data

Tamaki, S., Tomita, M., Suzuki, H. and Kanai, A.

Frontiers in Genetics (Frontiers in Genetics)  8 ( 227 )  2018.01

Research paper (scientific journal), Last author, Corresponding author, Accepted

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© 2018 Tamaki, Tomita, Suzuki and Kanai. To determine the mechanism underlying the flow of genetic information, it is important to understand the relationship between a tRNA and its binding enzyme, a member of the aminoacyl-tRNA synthetase (aaRS) family. We have developed a novel method to project the interacting regions of tRNA-aaRS complexes, obtained from their three-dimensional structures, onto two-dimensional space. The interacting surface between each tRNA and its aaRS was successfully identified by determining these interactions with an atomic distance threshold of 3.3 Å. We analyzed their interactions, using 60 mainly bacterial and eukaryotic tRNA-aaRS complexes, and showed that the tRNA sequence regions that interacted most strongly with each aaRS are the anticodon loop and the CCA terminal region, followed by the D-stem. A sequence conservation analysis of the canonical tRNAs was conducted in 83 bacterial, 182 archaeal, and 150 eukaryotic species. Our results show that the three tRNA regions that interact with the aaRS and two additional loop regions (D-loop and TψC-loop) known to be important for formation of the tRNA L-shaped structure are broadly conserved. We also found sequence conservations near the tRNA discriminator in the Bacteria and Archaea, and an enormous number of noncanonical tRNAs in the Eukaryotes. This is the first global view of tRNA evolution based on its structure and an unprecedented number of sequence data.

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Evolutionary analysis of HIV-1 Pol proteins reveals representative residues for viral subtype differentiation

Nagata, S., Imai, J., Makino, G., Tomita, M. and Kanai, A.

Frontiers in Microbiology 8 ( 2151 )  2017.11

Research paper (scientific journal), Joint Work, Accepted

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An archaeal RNA binding protein, FAU-1, is a novel ribonuclease related to rRNA stability in Pyrococcus and Thermococcus.

Ikeda, Y., Okada, Y., Sato, A., Kanai, T., Tomita, M., Atomi, H. and Kanai, A.

Scientific Reports 7   12674 2017.10

Research paper (scientific journal), Joint Work, Accepted

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Distinct requirements for energy metabolism in mouse primordial germ cells and their reprogramming to embryonic germ cells.

Hayashi, Y., Otsuka, K., Ebina, M., Igarashi, K., Takehara, A., Matsumoto, M., Kanai, A., Igarashi, K., Soga, T. and Matsui, Y.

Proceedings of the National Academy of Sciences. U. S. A. 114 ( 31 ) 8289 - 8294 2017.08

Research paper (scientific journal), Joint Work, Accepted

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Involvement of nucleotide diphosphate kinase 2 in the reopening of the sensitive period of filial imprinting of domestic chicks (Gallus gallus domesticus).

Yamaguchi, S., Aoki, N., Takehara, A., Mori, M., Kanai, A., Matsushima, T. and Homma, K. J.

Neuroscience Letters (Elsevier)  612   32 - 37 2016

Research paper (scientific journal), Joint Work, Accepted

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Precise mapping and dynamics of tRNA-derived fragments (tRFs) in the development of Triops cancriformis (tadpole shrimp).

Hirose, Y., Ikeda, T. K., Noro, E., Hiraoka, K., Tomita, M. and Kanai, A.

BMC Genetics (BioMed Central)  16 ( 83 )  2015.07

Research paper (scientific journal), Joint Work, Last author, Corresponding author, Accepted

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Background
In a deep sequencing analysis of small RNAs prepared from a living fossil, the tadpole shrimp Triops cancriformis, a 32-nt small RNA was specifically detected in the adult stage. A nucleotide sequence comparison between the 32-nt small RNA and predicted tRNA sequences in the draft nuclear genomic DNA showed that the small RNA was derived from tRNAGly(GCC). To determine the overall features of the tRNA-derived fragments (tRFs) of T. cancriformis, the small RNA sequences in each of the six developmental stages (egg, 1st − 4th instar larvae, and adult) were compared with the mitochondrial and nuclear tRNA sequences.

Results
We found that the tRFs were derived from mitochondrial and nuclear tRNAs corresponding to 16 and 39 anticodons, respectively. The total read number of nuclear tRFs was approximately 400 times larger than the number of mitochondrial tRFs. Interestingly, the main regions in each parental tRNA from which these tRFs were derived differed, depending on the parental anticodon. Mitochondrial tRFSer(GCU)s were abundantly produced from the 5’ half regions of the parental tRNA, whereas mitochondrial tRFVal(UAC)s were mainly produced from the 3’ end regions. Highly abundant nuclear tRFs, tRFGly(GCC)s, tRFGly(CCC)s, tRFGlu(CUC)s, and tRFLys(CUU)s were derived from the 5’ half regions of the parental tRNAs. Further analysis of the tRF read counts in the individual developmental stages suggested that the expression of mitochondrial and nuclear tRFs differed during the six stages. Based on these data, we precisely summarized the positions of the tRFs in their parental tRNAs and their expression changes during development.

Conclusions
Our results reveal the entire dynamics of the tRFs from both the nuclear and mitochondrial genomes of T. cancriformis and indicate that the majority of tRFs in the cell are derived from nuclear tRNAs. This study provides the first examples of developmentally expressed mitochondrial tRFs.

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Disrupted tRNA genes and tRNA fragments: a perspective on tRNA gene evolution.

Kanai, A.

Life (Basel) 5 ( 1 ) 321 - 331 2015.01

Research paper (scientific journal), Single Work, Accepted

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Analysis of genetic code ambiguity arising from nematode-specific misacylated tRNAs.

Hamashima, K., Mori, M., Andachi, Y., Tomita, M., Kohara, Y. and Kanai, A.

PLOS ONE 10 ( 1 ) e0116981 2015.01

Research paper (scientific journal), Joint Work, Accepted

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Effect of codon adaptation on codon-level and gene-level translation efficiency in vivo.

Nakahigashi, K., Takai, Y., Shiwa, Y., Wada, M., Honma, M., Yoshikawa, H., Tomita, M., Kanai, A. and Mori. H.

BMC Genomics 15 ( 1 ) 1115 2014.12

Research paper (scientific journal), Joint Work, Accepted

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Welcome to the new tRNA world!

Akio Kanai

Frontiers in Genetics 5   336 2014.09

Research paper (scientific journal), Single Work, Accepted

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tRNA gene diversity in the three domains of life

Fujishima, K. and Kanai, A.

Frontiers in Genetics 5   142 2014.04

Research paper (scientific journal), Joint Work, Accepted

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Identification of highly-disrupted tRNA genes in nuclear genome of the red alga, Cyanidioschyzon merolae 10D

Soma, A., Sugahara, J., Onodera, A., Yachie, N., Kanai, A., Watanabe, S., Yoshikawa, H., Ohnuma, M., Kuroiwa, H., Kuroiwa, T. and Sekine, Y.

Scientific Reports 3   2321 2013.07

Research paper (scientific journal), Joint Work, Accepted

Comprehensive computational analysis of bacterial CRP/FNR superfamily and its target motifs reveals stepwise evolution of transcriptional networks.

Matsui, M., Tomita, M. and Kanai, A.

Genome Biology and Evolution (Oxford Academic)  5 ( 2 ) 267 - 282 2013.02

Research paper (scientific journal), Joint Work, Last author, Corresponding author, Accepted

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The cAMP receptor protein (CRP)/fumarate and nitrate reduction regulatory protein (FNR)-type transcription factors (TFs) are members of a well-characterized global TF family in bacteria and have two conserved domains: the N-terminal ligand-binding domain for small molecules (e.g., cAMP, NO, or O2) and the C-terminal DNA-binding domain. Although the CRP/FNR-type TFs recognize very similar consensus DNA target sequences, they can regulate different sets of genes in response to environmental signals. To clarify the evolution of the CRP/FNR-type TFs throughout the bacterial kingdom, we undertook a comprehensive computational analysis of a large number of annotated CRP/FNR-type TFs and the corresponding bacterial genomes. Based on the amino acid sequence similarities among 1,455 annotated CRP/FNR-type TFs, spectral clustering classified the TFs into 12 representative groups, and stepwise clustering allowed us to propose a possible process of protein evolution. Although each cluster mainly consists of functionally distinct members (e.g., CRP, NTC, FNR-like protein, and FixK), FNR-related TFs are found in several groups and are distributed in a wide range of bacterial phyla in the sequence similarity network. This result suggests that the CRP/FNR-type TFs originated from an ancestral FNR protein, involved in nitrogen fixation. Furthermore, a phylogenetic profiling analysis showed that combinations of TFs and their target genes have fluctuated dynamically during bacterial evolution. A genome-wide analysis of TF-binding sites also suggested that the diversity of the transcriptional regulatory system was derived by the stepwise adaptation of TF-binding sites to the evolution of TFs.

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Alternative genetic code for amino acids and transfer RNA revisited

Hamashima, K. and Kanai, A.

Biomolecular Concepts 4 ( 3 ) 309-318 2013

Research paper (scientific journal), Joint Work, Accepted

Genomic heterogeneity in a natural archaeal population suggests a model of tRNA gene disruption

Sugahara, J., Fujishima, K., Nunoura, T., Takaki, Y., Takami, H., Takai, K., Tomita, M. and Kanai, A.

PLoS ONE 7 ( 3 ) e32504 2012.03

Research paper (scientific journal), Joint Work, Accepted

Metatranscriptomic analysis of microbes in an ocean-front deep subsurface hot spring reveals novel small RNAs and type-specific tRNA degradation

Murakami, S., Fujishima, K., Tomita, M. and Kanai, A.

Applied and Environmental Microbiology (American Society for Microbiology)  78 ( 4 ) 1015 - 1022 2012.02

Research paper (scientific journal), Joint Work, Last author, Corresponding author, Accepted

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Studies of small noncoding RNAs (sRNAs) have been conducted predominantly using culturable organisms, and the acquisition of further information about sRNAs from global environments containing uncultured organisms now is very important. In this study, hot spring water (57°C, pH 8.1) was collected directly from the underground environment at depths of 250 to 1,000 m in Yunohama, Japan, and small RNA sequences obtained from the environment were analyzed. A phylogenetic analysis of both archaeal and bacterial 16S rRNA gene sequences was conducted, and the results suggested the presence of unique species in the environment, corresponding to the Archaeal Richmond Mine Acidophilic Nanoorganisms (ARMAN) group and three new Betaproteobacteria. A metatranscriptomic analysis identified 64,194 (20,057 nonredundant) cDNA sequences. Of these cDNAs, 90% were either tRNAs, tRNA fragments, rRNAs, or rRNA fragments, whereas 2,181 reads (10%) were classified as previously uncharacterized putative candidate sRNAs. Among these, 15 were particularly abundant, 14 of which showed no sequence similarity to any known noncoding RNA, and at least six of which form very stable RNA secondary structures. The analysis of a large number of tRNA fragments suggested that unique relationships exist between the anticodons of the tRNAs and the sites of tRNA degradation. Previous bacterial tRNA degradation studies have been limited to specific organisms, such as Escherichia coli and Streptomyces coelicolor, and the current results suggest that specific tRNA decay occurs more frequently than previously expected.

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X-ray structure of the fourth type of archaeal tRNA splicing endonuclease: Insights into the evolution of a novel three-unit composition and a unique loop involved in broad substrate specificity.

Hirata, A., Fujishima, K., Yamagami, R., Kawamura, T., Banfield, JF., Kanai, A. and Hori, H.

Nucleic Acids Research 40 ( 20 ) 10554-10566 2012

Research paper (scientific journal), Joint Work, Accepted

GTP-dependent RNA 3'-terminal phosphate cyclase from the hyperthermophilic archaeon Pyrococcus furiosus

Sato, A., Soga, T., Igarashi, K., Takesue, K., Tomita, M. and Kanai, A.

Genes to Cells 16   1190-1199 2011.12

Research paper (scientific journal), Joint Work, Accepted