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2. Lack of membrane sex steroid receptors for mediating rapid endocrine responses in molluscan nervous systems.

Author

Fodor, István, Matsubara, Shin, Osugi, Tomohiro, Shiraishi, Akira, Kawada, Tsuyoshi, Satake, Honoo, and Pirger, Zsolt

Subjects
STEROID receptors, TRANSMEMBRANE domains, PROGESTERONE receptors, CELL membranes, ENDOCRINE system
Abstract

Despite the lack of endogenous synthesis and relevant nuclear receptors, several papers have been published over the decades claiming that the physiology of mollusks is affected by natural and synthetic sex steroids. With scant evidence for the existence of functional steroid nuclear receptors in mollusks, some scientists have speculated that the effects of steroids might be mediated via membrane receptors (i.e. via non-genomic/non-classical actions) - a mechanism that has been well-characterized in vertebrates. However, no study has yet investigated the ligand-binding ability of such receptor candidates in mollusks. The aim of the present study was to further trace the evolution of the endocrine system by investigating the presence of functional membrane sex steroid receptors in a mollusk, the great pond snail (Lymnaea stagnalis). We detected sequences homologous to the known vertebrate membrane sex steroid receptors in the Lymnaea transcriptome and genome data: G protein-coupled estrogen receptor-1 (GPER1); membrane progestin receptors (mPRs); G protein-coupled receptor family C group 6 member A (GPRC6A); and Zrt- and Irt-like protein 9 (ZIP9). Sequence analyses, including conserved domain analysis, phylogenetics, and transmembrane domain prediction, indicated that the mPR and ZIP9 candidates appeared to be homologs, while the GPER1 and GPRC6A candidates seemed to be non-orthologous receptors. All candidates transiently transfected into HEK293MSR cells were found to be localized at the plasma membrane, confirming that they function as membrane receptors. However, the signaling assays revealed that none of the candidates interacted with the main vertebrate steroid ligands. Our findings strongly suggest that functional membrane sex steroid receptors which would be homologous to the vertebrate ones are not present in Lymnaea. Although further experiments are required on other molluscan model species as well, we propose that both classical and non-classical sex steroid signaling for endocrine responses are specific to chordates, confirming that molluscan and vertebrate endocrine systems are fundamentally different. [ABSTRACT FROM AUTHOR]

Published
2024
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12. Contributors

Author

Amano, Masafumi, primary, Ando, Hironori, additional, Andoh, Tadashi, additional, Baker, Michael E., additional, Cameron, Melissa S., additional, Daubnerová, Ivana, additional, Donald, John A., additional, Fukumura, Keisuke, additional, Funaba, Masayuki, additional, Haraguchi, Shogo, additional, Hayakawa, Yoichi, additional, Hirako, Satoshi, additional, Hyodo, Susumu, additional, Iguchi, Taisen, additional, Inui, Akio, additional, Kaiya, Hiroyuki, additional, Kakizawa, Sho, additional, Kamiyama, Takumi, additional, Kanamori, Yohei, additional, Kanda, Shinji, additional, Katayama, Hidekazu, additional, Kato, Takashi, additional, Katsu, Yoshinao, additional, Katsuura, Goro, additional, Kawada, Tsuyoshi, additional, Kimura, Atsushi P., additional, Kitamura, Keiichiro, additional, Kobayashi, Yuki, additional, Kodani, Yu, additional, Konno, Norifumi, additional, Kuraku, Shigehiro, additional, Minakata, Hiroyuki, additional, Mita, Masatoshi, additional, Miyagawa, Shinichi, additional, Miyazato, Mikiya, additional, Mizusawa, Kanta, additional, Mori, Kenji, additional, Morishita, Fumihiro, additional, Moriyama, Shunsuke, additional, Nagasaki, Hiroshi, additional, Nagata, Shinji, additional, Nakamachi, Tomoya, additional, Niwa, Ryusuke, additional, Ogino, Yukiko, additional, Ogoshi, Maho, additional, Ohira, Tsuyoshi, additional, Ohki-Hamazaki, Hiroko, additional, Ohtaki, Hirokazu, additional, Ohyama, Yoshihiko, additional, Oka, Yoshitaka, additional, Okamoto, Naoki, additional, Onizawa, Moe, additional, Osugi, Tomohiro, additional, Saito, Yumiko, additional, Sakai, Takafumi, additional, Sakamoto, Hirotaka, additional, Sakamoto, Tatsuya, additional, Sakata, Ichiro, additional, Satake, Honoo, additional, Sato, Seiichi, additional, Sato, Tomomi, additional, Seike, Hitomi, additional, Sekiguchi, Toshio, additional, Shimizu, Munetaka, additional, Shinki, Toshimasa, additional, Shinoda, Tetsuro, additional, Shiomi, Kunihiro, additional, Suzuki, Nobuo, additional, Tachibana, Tetsuya, additional, Takahashi, Akiyoshi, additional, Takahashi, Toshio, additional, Takaoka, Akinori, additional, Takei, Yoshio, additional, Takenoya, Fumiko, additional, Takeuchi, Sakae, additional, Tanaka, Yoshiaki, additional, Toshinai, Koji, additional, Tsukada, Takehiro, additional, Tsutsui, Kazuyoshi, additional, Tsutsui, Naoaki, additional, Ubuka, Takayoshi, additional, Ukena, Kazuyoshi, additional, Wada, Nobuhiro, additional, Watanabe, Jun, additional, Wong, Marty Kwok-Shing, additional, Yamada, Taisho, additional, Yamaguchi, Yoko, additional, Yamanaka, Naoki, additional, Yamauchi, Kiyoshi, additional, Yuge, Shinya, additional, Zhou, Yijun, additional, and Žitňan, Dušan, additional

Published
2021
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15. Characterization of a novel species-specific 51-amino acid peptide, PEP51, as a caspase-3/7 activator in ovarian follicles of the ascidian, Ciona intestinalis Type A

Author

Sakai, Tsubasa, primary, Yamamoto, Tatsuya, additional, Watanabe, Takehiro, additional, Hozumi, Akiko, additional, Shiraishi, Akira, additional, Osugi, Tomohiro, additional, Matsubara, Shin, additional, Kawada, Tsuyoshi, additional, Sasakura, Yasunori, additional, Takahashi, Toshio, additional, and Satake, Honoo, additional

Published
2023
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16. Ovarian Follicle Development in Ascidians

Author

Satake, Honoo, primary, Kawada, Tsuyoshi, additional, Osugi, Tomohiro, additional, Sakai, Tsubasa, additional, Shiraishi, Akira, additional, Yamamoto, Tatsuya, additional, and Matsubara, Shin, additional

Published
2023
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18. Neuropeptide receptor transcriptome reveals unidentified neuroendocrine pathways.

Author

Yamanaka, Naoki, Yamamoto, Sachie, Zitnan, Dusan, Watanabe, Ken, Kawada, Tsuyoshi, Satake, Honoo, Kaneko, Yu, Hiruma, Kiyoshi, Tanaka, Yoshiaki, Shinoda, Tetsuro, and Kataoka, Hiroshi

Subjects
Neurosecretory Systems, Animals, Drosophila, Bombyx, Neuropeptides, Receptors, Neuropeptide, Ligands, Gene Expression Profiling, Reverse Transcriptase Polymerase Chain Reaction, Gene Expression, Larva, Receptors, Neuropeptide, General Science & Technology
Abstract

Neuropeptides are an important class of molecules involved in diverse aspects of metazoan development and homeostasis. Insects are ideal model systems to investigate neuropeptide functions, and the major focus of insect neuropeptide research in the last decade has been on the identification of their receptors. Despite these vigorous efforts, receptors for some key neuropeptides in insect development such as prothoracicotropic hormone, eclosion hormone and allatotropin (AT), remain undefined. In this paper, we report the comprehensive cloning of neuropeptide G protein-coupled receptors from the silkworm, Bombyx mori, and systematic analyses of their expression. Based on the expression patterns of orphan receptors, we identified the long-sought receptor for AT, which is thought to stimulate juvenile hormone biosynthesis in the corpora allata (CA). Surprisingly, however, the AT receptor was not highly expressed in the CA, but instead was predominantly transcribed in the corpora cardiaca (CC), an organ adjacent to the CA. Indeed, by using a reverse-physiological approach, we purified and characterized novel allatoregulatory peptides produced in AT receptor-expressing CC cells, which may indirectly mediate AT activity on the CA. All of the above findings confirm the effectiveness of a systematic analysis of the receptor transcriptome, not only in characterizing orphan receptors, but also in identifying novel players and hidden mechanisms in important biological processes. This work illustrates how using a combinatorial approach employing bioinformatic, molecular, biochemical and physiological methods can help solve recalcitrant problems in neuropeptide research.

Published
2008

20. Contributors

Author

Andrews, Paul L.R., Aslam, Ehsan, Barbe, Mary F., Bot, Ilze, Bright, F., Burgraff, Nicholas J., Byard, R.W., Chottova Dvorakova, Magdalena, Cinzia, Severini, Corrigan, Frances, Coveñas, Rafael, Ebner, Karl, Ebrahimi, Safieh, Erin, Nuray, Esteban, Francisco, Favila, Natalia, George, Rebecca, Gijasi, Asina, Grässel, Susanne, Gryszkiewicz, Weronika, Hashemy, Seyed Isaac, Hashim, Mariam, Heitman, Laura H., Hilliard, Brendan A., Kawada, Tsuyoshi, Kramer, Mark S., Krieg, Justin, Lee, Jiwon, Levick, Scott P., Marriott, Ian, Märtson, Anne-Grete, Mashaghi, Alireza, Mehboob, Riffat, Muñoz, Miguel, Nässel, Dick R., Niedermair, Tanja, Overton, Paul G., Pandey, Shashank, Park, Thomas J., Perner, Caroline, Ramirez, Jan-Marino, Rodríguez, Francisco D., Rosso, Marisa, Rudd, John A., Rupniak, Nadia M.J., Sanger, Gareth J., Satake, Honoo, Shiraishi, Akira, Singewald, Nicolas, Sipprell, Sophie E., Sorby-Adams, Annabel, Stanford, S.C., van Westen, Gerard J.P., van Wijk, Rob, Vink, Robert, Widiapradja, Alexander, Yoshiyama, Mitsuharu, and Zhao, Aishi

Published
2025
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29. List of Contributors

Author

Amano, Masafumi, primary, Ando, Hironori, additional, Andoh, Tadashi, additional, Daubnerova, Ivana, additional, Donald, John A., additional, Forgan, Leonard G., additional, Haraguchi, Shogo, additional, Hayakawa, Yoichi, additional, Hirako, Satoshi, additional, Hyodo, Susumu, additional, Iguchi, Taisen, additional, Inui, Akio, additional, Kageyama, Haruaki, additional, Kaiya, Hiroyuki, additional, Kakizawa, Sho, additional, Kanda, Shinji, additional, Kaneko, Hiroyuki, additional, Kataoka, Hiroshi, additional, Katayama, Hidekazu, additional, Kato, Takashi, additional, Katsu, Yoshinao, additional, Katsuura, Goro, additional, Kawada, Tsuyoshi, additional, Kimura, Atsushi P., additional, Kobayashi, Yuki, additional, Konno, Norifumi, additional, Konogami, Tadafumi, additional, Minakata, Hiroyuki, additional, Mita, Masatoshi, additional, Miyagawa, Shinichi, additional, Miyazato, Mikiya, additional, Mizoguchi, Akira, additional, Mizusawa, Kanta, additional, Mori, Kenji, additional, Morishita, Fumihiro, additional, Moriyama, Shunsuke, additional, Nagasaki, Hiroshi, additional, Nagata, Shinji, additional, Nakagawa, Yoshiaki, additional, Nakamachi, Tomoya, additional, Niimi, Teruyuki, additional, Ogino, Yukiko, additional, Ogoshi, Maho, additional, Ohira, Tsuyoshi, additional, Ohki-Hamazaki, Hiroko, additional, Ohtaki, Hirokazu, additional, Ohyama, Yoshihiko, additional, Oka, Yoshitaka, additional, Okamoto, Naoki, additional, Osugi, Tomohiro, additional, Park, Min Kyun, additional, Saito, Kazuki, additional, Saito, Yumiko, additional, Sakai, Takafumi, additional, Sakamoto, Hirotaka, additional, Sakamoto, Tatsuya, additional, Satake, Honoo, additional, Sato, Tomomi, additional, Sekiguchi, Toshio, additional, Shimizu, Munetaka, additional, Shinki, Toshimasa, additional, Shinoda, Tetsuro, additional, Sonobe, Haruyuki, additional, Suzuki, Koichi, additional, Suzuki, Nobuo, additional, Tachibana, Tetsuya, additional, Takahashi, Akiyoshi, additional, Takahashi, Toshio, additional, Takei, Yoshio, additional, Takenoya, Fumiko, additional, Takeuchi, Sakae, additional, Tanaka, Yoshiaki, additional, Tanizaki, Yuta, additional, Tsukada, Takehiro, additional, Tsukamoto, Yusuke, additional, Tsutsui, Kazuyoshi, additional, Tsutsui, Naoaki, additional, Ubuka, Takayoshi, additional, Ukena, Kazuyoshi, additional, Wada, Nobuhiro, additional, Watanabe, Jun, additional, Wong, Marty K.S., additional, Xu, Zhifang, additional, Yaginuma, Toshinobu, additional, Yamauchi, Kiyoshi, additional, Yuge, Shinya, additional, and Zitnan, Dusan, additional

Published
2016
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44. Tachykinins : Neuropeptides That Are Ancient, Diverse, Widespread and Functionally Pleiotropic

Author

Nässel, Dick R., Zandawala, Meet, Kawada, Tsuyoshi, Satake, Honoo, Nässel, Dick R., Zandawala, Meet, Kawada, Tsuyoshi, and Satake, Honoo

Abstract

Tachykinins (TKs) are ancient neuropeptides present throughout the bilaterians and are, with some exceptions, characterized by a conserved FX(1)GX(2)Ramide carboxy terminus among protostomes and FXGLMamide in deuterostomes. The best-known TK is the vertebrate substance P, which in mammals, together with other TKs, has been implicated in health and disease with important roles in pain, inflammation, cancer, depressive disorder, immune system, gut function, hematopoiesis, sensory processing, and hormone regulation. The invertebrate TKs are also known to have multiple functions in the central nervous system and intestine and these have been investigated in more detail in the fly Drosophila and some other arthropods. Here, we review the protostome and deuterostome organization and evolution of TK precursors, peptides and their receptors, as well as their functions, which appear to be partly conserved across Bilateria. We also outline the distribution of TKs in the brains of representative organisms. In Drosophila, recent studies have revealed roles of TKs in early olfactory processing, neuromodulation in circuits controlling locomotion and food search, nociception, aggression, metabolic stress, and hormone release. TK signaling also regulates lipid metabolism in the Drosophila intestine. In crustaceans, TK is an important neuromodulator in rhythm-generating motor circuits in the stomatogastric nervous system and a presynaptic modulator of photoreceptor cells. Several additional functional roles of invertebrate TKs can be inferred from their distribution in various brain circuits. In addition, there are a few interesting cases where invertebrate TKs are injected into prey animals as vasodilators from salivary glands or paralyzing agents from venom glands. In these cases, the peptides are produced in the glands of the predator with sequences mimicking the prey TKs. Lastly, the TK-signaling system appears to have duplicated in Panarthropoda (comprising arthropods, onychoph

Published
2019
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