A population of neurons that produce hugin and express the diuretic hormone 44 receptor gene projects to the corpora allata in Drosophila melanogaster
The corpora allata (CA) are essential endocrine organs that biosynthesize and secrete the sesquiterpenoid hormone, namely juvenile hormone (JH), to regulate a wide variety of developmental and physiological events in insects. CA are directly innervated with neurons in many insect species, implying t...
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creator | Mizuno, Yosuke Imura, Eisuke Kurogi, Yoshitomo Shimada‐Niwa, Yuko Kondo, Shu Tanimoto, Hiromu Hückesfeld, Sebastian Pankratz, Michael J. Niwa, Ryusuke |
description | The corpora allata (CA) are essential endocrine organs that biosynthesize and secrete the sesquiterpenoid hormone, namely juvenile hormone (JH), to regulate a wide variety of developmental and physiological events in insects. CA are directly innervated with neurons in many insect species, implying the innervations to be important for regulating JH biosynthesis. Although this is also true for the model organism Drosophila melanogaster, neurotransmitters produced in the CA‐projecting neurons are yet to be identified. In this study on D. melanogaster, we aimed to demonstrate that a subset of neurons producing the neuropeptide hugin, the invertebrate counterpart of the vertebrate neuromedin U, directly projects to the adult CA. A synaptic vesicle marker in the hugin neurons was observed at their axon termini located on the CA, which were immunolabeled with a newly‐generated antibody to the JH biosynthesis enzyme JH acid O‐methyltransferase. We also found the CA‐projecting hugin neurons to likely express a gene encoding the specific receptor for diuretic hormone 44 (Dh44). Moreover, our data suggest that the CA‐projecting hugin neurons have synaptic connections with the upstream neurons producing Dh44. Unexpectedly, the inhibition of CA‐projecting hugin neurons did not significantly alter the expression levels of the JH‐inducible gene Krüppel‐homolog 1, which implies that the CA‐projecting neurons are not involved in JH biosynthesis but rather in other known biological processes. This is the first study to identify a specific neurotransmitter of the CA‐projecting neurons in D. melanogaster, and to anatomically characterize a neuronal pathway of the CA‐projecting neurons and their upstream neurons.
The corpus allatum is an essential endocrine organ that biosynthesizes and secretes juvenile hormone, which regulates a wide variety of developmental and physiological events in insects. The study using the fruit fly Drosophila melanogaster shows that a subset of neurons producing the neuropeptide hugin, an invertebrate counterpart of the vertebrate neuromedin U, directly projects to the adult corpus allatum. |
doi_str_mv | 10.1111/dgd.12733 |
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The corpus allatum is an essential endocrine organ that biosynthesizes and secretes juvenile hormone, which regulates a wide variety of developmental and physiological events in insects. The study using the fruit fly Drosophila melanogaster shows that a subset of neurons producing the neuropeptide hugin, an invertebrate counterpart of the vertebrate neuromedin U, directly projects to the adult corpus allatum.</description><identifier>ISSN: 0012-1592</identifier><identifier>EISSN: 1440-169X</identifier><identifier>DOI: 10.1111/dgd.12733</identifier><identifier>PMID: 34021588</identifier><language>eng</language><publisher>Japan: Wiley Subscription Services, Inc</publisher><subject>Animals ; Biosynthesis ; Corpora Allata ; diuretic hormone 44 ; Diuretics ; Drosophila melanogaster ; Drosophila melanogaster - genetics ; hugin ; Insects ; Invertebrates ; juvenile hormone ; Juvenile Hormones ; Methyltransferase ; Neuromedin ; Neurons ; Neurotransmitters ; Synapses</subject><ispartof>Development, growth & differentiation, 2021-05, Vol.63 (4-5), p.249-261</ispartof><rights>2021 Japanese Society of Developmental Biologists</rights><rights>2021 Japanese Society of Developmental Biologists.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3883-7f68fba62c28daf940fd6f4251a3d818c8b4d7ed016536d7352a9593f0370e0e3</citedby><cites>FETCH-LOGICAL-c3883-7f68fba62c28daf940fd6f4251a3d818c8b4d7ed016536d7352a9593f0370e0e3</cites><orcidid>0000-0001-5880-6064 ; 0000-0003-0236-6375 ; 0000-0001-5458-6471 ; 0000-0002-4625-8379 ; 0000-0002-1716-455X ; 0000-0001-5757-4329</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fdgd.12733$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fdgd.12733$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34021588$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mizuno, Yosuke</creatorcontrib><creatorcontrib>Imura, Eisuke</creatorcontrib><creatorcontrib>Kurogi, Yoshitomo</creatorcontrib><creatorcontrib>Shimada‐Niwa, Yuko</creatorcontrib><creatorcontrib>Kondo, Shu</creatorcontrib><creatorcontrib>Tanimoto, Hiromu</creatorcontrib><creatorcontrib>Hückesfeld, Sebastian</creatorcontrib><creatorcontrib>Pankratz, Michael J.</creatorcontrib><creatorcontrib>Niwa, Ryusuke</creatorcontrib><title>A population of neurons that produce hugin and express the diuretic hormone 44 receptor gene projects to the corpora allata in Drosophila melanogaster</title><title>Development, growth & differentiation</title><addtitle>Dev Growth Differ</addtitle><description>The corpora allata (CA) are essential endocrine organs that biosynthesize and secrete the sesquiterpenoid hormone, namely juvenile hormone (JH), to regulate a wide variety of developmental and physiological events in insects. CA are directly innervated with neurons in many insect species, implying the innervations to be important for regulating JH biosynthesis. Although this is also true for the model organism Drosophila melanogaster, neurotransmitters produced in the CA‐projecting neurons are yet to be identified. In this study on D. melanogaster, we aimed to demonstrate that a subset of neurons producing the neuropeptide hugin, the invertebrate counterpart of the vertebrate neuromedin U, directly projects to the adult CA. A synaptic vesicle marker in the hugin neurons was observed at their axon termini located on the CA, which were immunolabeled with a newly‐generated antibody to the JH biosynthesis enzyme JH acid O‐methyltransferase. We also found the CA‐projecting hugin neurons to likely express a gene encoding the specific receptor for diuretic hormone 44 (Dh44). Moreover, our data suggest that the CA‐projecting hugin neurons have synaptic connections with the upstream neurons producing Dh44. Unexpectedly, the inhibition of CA‐projecting hugin neurons did not significantly alter the expression levels of the JH‐inducible gene Krüppel‐homolog 1, which implies that the CA‐projecting neurons are not involved in JH biosynthesis but rather in other known biological processes. This is the first study to identify a specific neurotransmitter of the CA‐projecting neurons in D. melanogaster, and to anatomically characterize a neuronal pathway of the CA‐projecting neurons and their upstream neurons.
The corpus allatum is an essential endocrine organ that biosynthesizes and secretes juvenile hormone, which regulates a wide variety of developmental and physiological events in insects. The study using the fruit fly Drosophila melanogaster shows that a subset of neurons producing the neuropeptide hugin, an invertebrate counterpart of the vertebrate neuromedin U, directly projects to the adult corpus allatum.</description><subject>Animals</subject><subject>Biosynthesis</subject><subject>Corpora Allata</subject><subject>diuretic hormone 44</subject><subject>Diuretics</subject><subject>Drosophila melanogaster</subject><subject>Drosophila melanogaster - genetics</subject><subject>hugin</subject><subject>Insects</subject><subject>Invertebrates</subject><subject>juvenile hormone</subject><subject>Juvenile Hormones</subject><subject>Methyltransferase</subject><subject>Neuromedin</subject><subject>Neurons</subject><subject>Neurotransmitters</subject><subject>Synapses</subject><issn>0012-1592</issn><issn>1440-169X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kU9LHDEYh0NR6mp78AuUgJf2MJq_M5mjuFYFoZcWehuyyZvdWWaSaTLB-kX8vEZXPQjmEkie98kv_BA6puSUlnVm1_aUsobzT2hBhSAVrdu_e2hBCGUVlS07QIcpbQkhQlD2GR1wQRiVSi3QwzmewpQHPffB4-CwhxyDT3je6BlPMdhsAG_yuvdYe4vh_xQhPV0Dtn2OMPcGb0IcgwcsBI5gYJpDxGsoB2V-C2YueHieMCFOIWqsh_KgxsW5jCGFadMPGo8waB_WOs0Qv6B9p4cEX1_2I_Tn5-Xvi-vq9tfVzcX5bWW4UrxqXK3cStfMMGW1awVxtnaCSaq5VVQZtRK2AUtoLXltGy6ZbmXLHeENAQL8CH3feUvSfxnS3I19MlDieQg5dUxyyqgiTBX05B26DTn6kq5QQrYNbYks1I8dZcrHUgTXTbEfdbzvKOmeyupKWd1zWYX99mLMqxHsG_naTgHOdsBdP8D9x6ZuebXcKR8BsgCfdw</recordid><startdate>202105</startdate><enddate>202105</enddate><creator>Mizuno, Yosuke</creator><creator>Imura, Eisuke</creator><creator>Kurogi, Yoshitomo</creator><creator>Shimada‐Niwa, Yuko</creator><creator>Kondo, Shu</creator><creator>Tanimoto, Hiromu</creator><creator>Hückesfeld, Sebastian</creator><creator>Pankratz, Michael J.</creator><creator>Niwa, Ryusuke</creator><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-5880-6064</orcidid><orcidid>https://orcid.org/0000-0003-0236-6375</orcidid><orcidid>https://orcid.org/0000-0001-5458-6471</orcidid><orcidid>https://orcid.org/0000-0002-4625-8379</orcidid><orcidid>https://orcid.org/0000-0002-1716-455X</orcidid><orcidid>https://orcid.org/0000-0001-5757-4329</orcidid></search><sort><creationdate>202105</creationdate><title>A population of neurons that produce hugin and express the diuretic hormone 44 receptor gene projects to the corpora allata in Drosophila melanogaster</title><author>Mizuno, Yosuke ; Imura, Eisuke ; Kurogi, Yoshitomo ; Shimada‐Niwa, Yuko ; Kondo, Shu ; Tanimoto, Hiromu ; Hückesfeld, Sebastian ; Pankratz, Michael J. ; Niwa, Ryusuke</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3883-7f68fba62c28daf940fd6f4251a3d818c8b4d7ed016536d7352a9593f0370e0e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Biosynthesis</topic><topic>Corpora Allata</topic><topic>diuretic hormone 44</topic><topic>Diuretics</topic><topic>Drosophila melanogaster</topic><topic>Drosophila melanogaster - genetics</topic><topic>hugin</topic><topic>Insects</topic><topic>Invertebrates</topic><topic>juvenile hormone</topic><topic>Juvenile Hormones</topic><topic>Methyltransferase</topic><topic>Neuromedin</topic><topic>Neurons</topic><topic>Neurotransmitters</topic><topic>Synapses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mizuno, Yosuke</creatorcontrib><creatorcontrib>Imura, Eisuke</creatorcontrib><creatorcontrib>Kurogi, Yoshitomo</creatorcontrib><creatorcontrib>Shimada‐Niwa, Yuko</creatorcontrib><creatorcontrib>Kondo, Shu</creatorcontrib><creatorcontrib>Tanimoto, Hiromu</creatorcontrib><creatorcontrib>Hückesfeld, Sebastian</creatorcontrib><creatorcontrib>Pankratz, Michael J.</creatorcontrib><creatorcontrib>Niwa, Ryusuke</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Development, growth & differentiation</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mizuno, Yosuke</au><au>Imura, Eisuke</au><au>Kurogi, Yoshitomo</au><au>Shimada‐Niwa, Yuko</au><au>Kondo, Shu</au><au>Tanimoto, Hiromu</au><au>Hückesfeld, Sebastian</au><au>Pankratz, Michael J.</au><au>Niwa, Ryusuke</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A population of neurons that produce hugin and express the diuretic hormone 44 receptor gene projects to the corpora allata in Drosophila melanogaster</atitle><jtitle>Development, growth & differentiation</jtitle><addtitle>Dev Growth Differ</addtitle><date>2021-05</date><risdate>2021</risdate><volume>63</volume><issue>4-5</issue><spage>249</spage><epage>261</epage><pages>249-261</pages><issn>0012-1592</issn><eissn>1440-169X</eissn><abstract>The corpora allata (CA) are essential endocrine organs that biosynthesize and secrete the sesquiterpenoid hormone, namely juvenile hormone (JH), to regulate a wide variety of developmental and physiological events in insects. CA are directly innervated with neurons in many insect species, implying the innervations to be important for regulating JH biosynthesis. Although this is also true for the model organism Drosophila melanogaster, neurotransmitters produced in the CA‐projecting neurons are yet to be identified. In this study on D. melanogaster, we aimed to demonstrate that a subset of neurons producing the neuropeptide hugin, the invertebrate counterpart of the vertebrate neuromedin U, directly projects to the adult CA. A synaptic vesicle marker in the hugin neurons was observed at their axon termini located on the CA, which were immunolabeled with a newly‐generated antibody to the JH biosynthesis enzyme JH acid O‐methyltransferase. We also found the CA‐projecting hugin neurons to likely express a gene encoding the specific receptor for diuretic hormone 44 (Dh44). Moreover, our data suggest that the CA‐projecting hugin neurons have synaptic connections with the upstream neurons producing Dh44. Unexpectedly, the inhibition of CA‐projecting hugin neurons did not significantly alter the expression levels of the JH‐inducible gene Krüppel‐homolog 1, which implies that the CA‐projecting neurons are not involved in JH biosynthesis but rather in other known biological processes. This is the first study to identify a specific neurotransmitter of the CA‐projecting neurons in D. melanogaster, and to anatomically characterize a neuronal pathway of the CA‐projecting neurons and their upstream neurons.
The corpus allatum is an essential endocrine organ that biosynthesizes and secretes juvenile hormone, which regulates a wide variety of developmental and physiological events in insects. The study using the fruit fly Drosophila melanogaster shows that a subset of neurons producing the neuropeptide hugin, an invertebrate counterpart of the vertebrate neuromedin U, directly projects to the adult corpus allatum.</abstract><cop>Japan</cop><pub>Wiley Subscription Services, Inc</pub><pmid>34021588</pmid><doi>10.1111/dgd.12733</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-5880-6064</orcidid><orcidid>https://orcid.org/0000-0003-0236-6375</orcidid><orcidid>https://orcid.org/0000-0001-5458-6471</orcidid><orcidid>https://orcid.org/0000-0002-4625-8379</orcidid><orcidid>https://orcid.org/0000-0002-1716-455X</orcidid><orcidid>https://orcid.org/0000-0001-5757-4329</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Biosynthesis Corpora Allata diuretic hormone 44 Diuretics Drosophila melanogaster Drosophila melanogaster - genetics hugin Insects Invertebrates juvenile hormone Juvenile Hormones Methyltransferase Neuromedin Neurons Neurotransmitters Synapses |
title | A population of neurons that produce hugin and express the diuretic hormone 44 receptor gene projects to the corpora allata in Drosophila melanogaster |
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