Papers - Atsushi UGAJIN
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Takayuki Watanabe, Atsushi Ugajin, Kosuke Tateishi, Hidehiro Watanabe, Makoto Mizunami
Scientific Reports 15 ( 1 ) 3949 2025.01
Language：English Publishing type：Research paper (scientific journal) Publisher：Springer Science and Business Media LLC
DOI： 10.1038/s41598-025-87978-6
Other Link： https://www.nature.com/articles/s41598-025-87978-6
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Identification and in vivo functional analysis of furanocoumarin-responsive cytochrome P450s in a Rutaceae-feeding Papilio butterfly Reviewed
Rei Miyashita, Atsushi Ugajin, Hiroki Oda, Katsuhisa Ozaki
Journal of Experimental Biology 227 ( 16 ) jeb247791 2024.07
Authorship：Lead author, Corresponding author Language：English Publishing type：Research paper (scientific journal)
DOI： 10.1242/jeb.247791
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Kosuke Tateishi, Takayuki Watanabe, Mana Domae, Atsushi Ugajin, Hiroshi Nishino, Hiroyuki Nakagawa, Makoto Mizunami, Hidehiro Watanabe
PNAS Nexus pgae162 2024.04
Language：English Publishing type：Research paper (scientific journal)
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Genes associated with hot defensive bee ball in the Japanese honeybee, Apis cerana japonica Reviewed
Kamioka T, Suzuki H, Ugajin A, Yamaguchi Y, Nishimura M, Sasaki T, Ono M, Kawata M
BMC Ecology and Evolution 22 ( 31 ) 2022.03
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Ugajin A*, Ozaki K
Frontiers in Insect Science 1 696179 2021.07
Authorship：Lead author, Corresponding author Language：English Publishing type：Research paper (scientific journal)
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Caste-specific development of the dopaminergic system during metamorphosis in female honey bees Reviewed
Sasaki K, Ugajin A, Harano K
PLoS ONE 13 ( 10 ) e0206624 2018.10
Language：English Publishing type：Research paper (scientific journal)
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Immediate-early promoter-driven transgenic reporter system for neuroethological researches in a hemimetabolous insect Reviewed
Watanabe T, Ugajin A, Aonuma H
eNeuro 0061-18 2018.08
Language：English
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Yamaguchi Y, Ugajin A, Utagawa S, Nishimura M, Hattori M, Ono M
Behavioral Ecology and Sociobiology 72 ( 8 ) 123 2018.07
Authorship：Lead author, Corresponding author Language：English Publishing type：Research paper (scientific journal)
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A. Ugajin*, H. Uchiyama, T. Miyata, T. Sasaki, S. Yajima, M. Ono
Insect Molecular Biology 27 ( 2 ) 154 - 165 2018.04
Authorship：Lead author, Corresponding author Language：English Publishing type：Research paper (scientific journal) Publisher：Blackwell Publishing Ltd
Despite possessing a limited number of neurones compared to vertebrates, honeybees show remarkable learning and memory performance, an example being ‘dance communication’. In this phenomenon, foraging honeybees learn the location of a newly discovered food source and transmit the information to nestmates by symbolic abdomen vibrating behaviour, leading to navigation of nestmates to the new food source. As an initial step toward understanding the detailed molecular mechanisms underlying the sophisticated learning and memory performance of the honeybee, we focused on the neural immediate early genes (IEGs), which are specific genes quickly transcribed after neural activity without de novo protein synthesis. Although these have been reported to play an essential role in learning and memory processes in vertebrates, far fewer studies have been performed in insects in this regard. From RNA-sequencing analysis and subsequent assays, we identified three genes, Src homology 3 (SH3) domain binding kinase, family with sequence similarity 46 and GB47136, as novel neural IEGs in the honeybee. Foragers and/or orientating bees, which fly around their hives to memorize the positional information, showed induced expression of these IEGs in the mushroom body, a higher-order centre essential for learning and memory, indicating a possible role for the novel IEGs in foraging-related learning and memory processes in the honeybee.
DOI： 10.1111/imb.12355
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Matsuo K, Kubo R, Sasaki T, Ono M, Ugajin A
Apidologie 49 ( 3 ) 411 - 414 2018.03
Authorship：Last author, Corresponding author Language：English Publishing type：Research paper (scientific journal)
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Atsuhiro Yamane, Hiroki Kohno, Tsubomi Ikeda, Kumi Kaneko, Atsushi Ugajin, Toshiyuki Fujita, Takekazu Kunieda, Takeo Kubo
PLOS ONE 12 ( 5 ) e0176809 2017.05
Language：English Publisher：PUBLIC LIBRARY SCIENCE
In insect brains, the mushroom bodies (MBs, a higher center) comprise intrinsic neurons, termed Kenyon cells (KCs). We previously showed that the honeybee (Apis mellifera L.) MBs comprise four types of KCs, in addition to the previously known three types of KCs: class I large-type KCs (lKCs), class I small-type KCs (sKCs) and class II KCs, novel class I 'middle-type' KCs (mKCs), which are characterized by the preferential expression of a gene, termed mKast. Although mKast was originally discovered during the search for genes whose expression is enriched in the optic lobes (OLs) in the worker brain, subsequent analysis revealed that the gene is expressed in an mKC-preferential manner in the MBs. To gain more insights into the function of mKast in the honeybee brain, we here performed expression analysis of mKast and immunohistochemistry of the mKast protein. Prominent mKast expression was first detected in the brain after the P7 pupal stage. In addition, mKast was expressed almost selectively in the brain, suggesting its late pupal and adult specific functions in the brain. Immunohistochemistry revealed that mKast-like immunoreactivity is detected in several regions in the worker brain: inside and around the MB calyces, at the outer edges of the OL lobula, at the outer surface of and posterior to the antennal lobes (ALs), along the dorsal midline of the anterior brain and at the outer surface of the subesophageal ganglions (SOG). mKast-like immunoreactivities in the MBs, OLs, ALs and SOG were due to the corresponding neurons, while mKast-like immunoreactivities beneath/between the MB calyces were assumed to most likely correspond to the lateral/medial neurosecretory cells.
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Ryohei Kubo, Atsushi Ugajin, Masato Ono
APPLIED ENTOMOLOGY AND ZOOLOGY 51 ( 4 ) 549 - 554 2016.11
Language：English Publishing type：Research paper (scientific journal) Publisher：SPRINGER JAPAN KK
We identified mermithid nematodes infecting a post-hibernating Japanese bumblebee (Bombus pseudobaicalensis Vogt) queen in Nemuro, Hokkaido, Japan. The infected queen did not lay eggs or feed on pollen during laboratory rearing. In addition, the queen usually crawled under the straw set in the rearing box, which differed from the typical behavior of a normal queen. Intra-abdominal observation revealed that, compared with the ovaries of a normal queen, those of the infected queen were undeveloped. Infection by mermithid nematodes may result in the sterilization of the bumblebee queen. The molecular phylogenetic analysis revealed that the mermithid species infecting the Japanese bumblebee queen differed from the Pheromermis species reported as a parasite of Hymenopteran insects, and that they were closely related to mermithid nematodes found in spiders and Ovomermis sinensis Chen, a parasite of the tobacco budworm larva Helicoverpa armigera Hubner. These findings constitute the first report of mermithid nematodes infecting Japanese bumblebee.
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Atsushi Ugajin, Takayuki Watanabe, Hironobu Uchiyama, Tetsuhiko Sasaki, Shunsuke Yajima, Masato Ono
BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 478 ( 2 ) 1014 - 1019 2016.09
Authorship：Lead author, Corresponding author Language：English Publishing type：Research paper (scientific journal) Publisher：ACADEMIC PRESS INC ELSEVIER SCIENCE
Specific genes quickly transcribed after extracellular stimuli without de novo protein synthesis are known as immediate early genes (IEGs) and are thought to contribute to learning and memory processes in the mature nervous system of vertebrates. A recent study revealed that the homolog of Early growth response protein-1 (Egr-1), which is one of the best-characterized vertebrate IEGs, shared similar properties as a neural activity-dependent gene in the adult brain of insects. With regard to the roles of vertebrate Egr-1 in neural development, the contribution to the development and growth of visual systems has been reported. However, in insects, the expression dynamics of the Egr-1 homologous gene during neural development remains poorly understood. Our expression analysis demonstrated that AmEgr, a honeybee homolog of Egr-1, was transiently upregulated in the developing brain during the early to mid pupal stages. In situ hybridization and 5-bromo-2'-deoxyuridine (BrdU) immunohistochemistry revealed that AmEgr was mainly expressed in post-mitotic cells in optic lobes, the primary visual center of the insect brain. These findings suggest the evolutionarily conserved role of Egr homologs in the development of visual systems in vertebrates and insects. (C) 2016 Elsevier Inc. All rights reserved.
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Expression profile of the sex determination gene doublesex in a gynandromorph of bumblebee, Bombus ignitus Reviewed
Atsushi Ugajin, Koshiro Matsuo, Ryohei Kubo, Tetsuhiko Sasaki, Masato Ono
SCIENCE OF NATURE 103 ( 3-4 ) 17 2016
Authorship：Lead author, Corresponding author Language：English Publishing type：Research paper (scientific journal) Publisher：SPRINGER HEIDELBERG
Gynandromorphy that has both male and female features is known in many insect orders, including Hymenoptera. In most cases, however, only external morphology and behavioral aspects have been studied. We found a gynandromorph of bumblebee, Bombus ignitus, that showed almost bilateral distribution of external sexual traits, with male characters observed on the left side and female characters on the right side. This individual never exhibited sexual behavior toward new queens. The dissection of the head part showed that it had bilaterally dimorphic labial glands, only the left of which was well developed and synthesized male-specific pheromone components. In contrast, the gynandromorph possessed an ovipositor and a pair of ovaries in the abdominal part, suggesting that it had a uniformly female reproductive system. Furthermore, we characterized several internal organs of the gynandromorph by a molecular biological approach. The expression analyses of a sex determination gene, doublesex, in the brain, the fat bodies, the hindgut, and the ovaries of the gynandromorph revealed a male-type expression pattern exclusively in the left brain hemisphere and consistent female-type expression in other tissues. These findings clearly indicate the sexual discordance between external traits and internal organs in the gynandromorph. The results of genetic analyses using microsatellite markers suggested that this individual consisted of both genetically male-and female-type tissues.
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Identification and characterization of an Egr ortholog as a neural immediate early gene in the European honeybee (Apis mellifera L.) Reviewed
Atsushi Ugajin, Takekazu Kunieda, Takeo Kubo
FEBS LETTERS 587 ( 19 ) 3224 - 3230 2013.10
Authorship：Lead author Language：English Publishing type：Research paper (scientific journal) Publisher：ELSEVIER SCIENCE BV
To date, there are only few reports of immediate early genes (IEGs) available in insects. Aiming at identifying a conserved IEG in insects, we characterized an Egr homolog of the honeybee (AmEgr: Apis mellifera Egr). AmEgr was transiently induced in whole worker brains after seizure induction. In situ hybridization for AmEgr indicated that neural activity of a certain mushroom body (a higher brain center) neuron subtype, which is the same as that we previously identified using another non-coding IEG, termed kakusei, is more enhanced in forager brains. These findings suggest that Egr can be utilized as an IEG in insects. (C) 2013 Federation of European Biochemical Societies. Published by Elsevier B. V. All rights reserved.
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Novel Middle-Type Kenyon Cells in the Honeybee Brain Revealed by Area-Preferential Gene Expression Analysis Reviewed
Kumi Kaneko, Tsubomi Ikeda, Mirai Nagai, Sayaka Hori, Chie Umatani, Hiroto Tadano, Atsushi Ugajin, Takayoshi Nakaoka, Rajib Kumar Paul, Tomoko Fujiyuki, Kenichi Shirai, Takekazu Kunieda, Hideaki Takeuchi, Takeo Kubo
PLOS ONE 8 ( 8 ) e71732 2013.08
Language：English Publishing type：Research paper (scientific journal) Publisher：PUBLIC LIBRARY SCIENCE
The mushroom bodies (a higher center) of the honeybee (Apis mellifera L) brain were considered to comprise three types of intrinsic neurons, including large- and small-type Kenyon cells that have distinct gene expression profiles. Although previous neural activity mapping using the immediate early gene kakusei suggested that small-type Kenyon cells are mainly active in forager brains, the precise Kenyon cell types that are active in the forager brain remain to be elucidated. We searched for novel gene(s) that are expressed in an area-preferential manner in the honeybee brain. By identifying and analyzing expression of a gene that we termed mKast (middle-type Kenyon cell-preferential arrestin-related protein), we discovered novel 'middle-type Kenyon cells' that are sandwiched between large- and small-type Kenyon cells and have a gene expression profile almost complementary to those of large- and small-type Kenyon cells. Expression analysis of kakusei revealed that both small-type Kenyon cells and some middle-type Kenyon cells are active in the forager brains, suggesting their possible involvement in information processing during the foraging flight. mKast expression began after the differentiation of small- and large-type Kenyon cells during metamorphosis, suggesting that middle-type Kenyon cells differentiate by modifying some characteristics of large- and/or small-type Kenyon cells. Interestingly, CaMKII and mKast, marker genes for large- and middle-type Kenyon cells, respectively, were preferentially expressed in a distinct set of optic lobe (a visual center) neurons. Our findings suggested that it is not simply the Kenyon cell-preferential gene expression profiles, rather, a 'clustering' of neurons with similar gene expression profiles as particular Kenyon cell types that characterize the honeybee mushroom body structure.
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Identification of kakusei, a Nuclear Non-Coding RNA, as an Immediate Early Gene from the Honeybee, and Its Application for Neuroethological Study Reviewed
Taketoshi Kiya, Atsushi Ugajin, Takekazu Kunieda, Takeo Kubo
INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES 13 ( 12 ) 15496 - 15509 2012.12
Language：English Publisher：MDPI AG
The honeybee is a social insect that exhibits various social behaviors. To elucidate the neural basis of honeybee behavior, we detected neural activity in freely-moving honeybee workers using an immediate early gene (IEG) that is expressed in a neural activity-dependent manner. In European honeybees (Apis mellifera), we identified a novel nuclear non-coding RNA, termed kakusei, as the first insect IEG, and revealed the neural activity pattern in foragers. In addition, we isolated a homologue of kakusei, termed Acks, from the Japanese honeybee (Apis cerana), and detected active neurons in workers fighting with the giant hornet.
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Detection of Neural Activity in the Brains of Japanese Honeybee Workers during the Formation of a "Hot Defensive Bee Ball" Reviewed
Atsushi Ugajin, Taketoshi Kiya, Takekazu Kunieda, Masato Ono, Tadaharu Yoshida, Takeo Kubo
PLOS ONE 7 ( 3 ) e32902 2012.03
Authorship：Lead author Language：English Publishing type：Research paper (scientific journal) Publisher：PUBLIC LIBRARY SCIENCE
Anti-predator behaviors are essential to survival for most animals. The neural bases of such behaviors, however, remain largely unknown. Although honeybees commonly use their stingers to counterattack predators, the Japanese honeybee (Apis cerana japonica) uses a different strategy to fight against the giant hornet (Vespa mandarinia japonica). Instead of stinging the hornet, Japanese honeybees form a "hot defensive bee ball" by surrounding the hornet en masse, killing it with heat. The European honeybee (A. mellifera ligustica), on the other hand, does not exhibit this behavior, and their colonies are often destroyed by a hornet attack. In the present study, we attempted to analyze the neural basis of this behavior by mapping the active brain regions of Japanese honeybee workers during the formation of a hot defensive bee ball. First, we identified an A. cerana homolog Acks = Apis cerana kakusei of kakusei, an immediate early gene that we previously identified from A. mellifera, and showed that Acks has characteristics similar to kakusei and can be used to visualize active brain regions in A. cerana. Using Acks as a neural activity marker, we demonstrated that neural activity in the mushroom bodies, especially in Class II Kenyon cells, one subtype of mushroom body intrinsic neurons, and a restricted area between the dorsal lobes and the optic lobes was increased in the brains of Japanese honeybee workers involved in the formation of a hot defensive bee ball. In addition, workers exposed to 46 degrees C heat also exhibited Acks expression patterns similar to those observed in the brains of workers involved in the formation of a hot defensive bee ball, suggesting that the neural activity observed in the brains of workers involved in the hot defensive bee ball mainly reflects thermal stimuli processing.