Calcitonin receptor signaling in the medial preoptic area enables risk-taking maternal care
Maternal mammals exhibit heightened motivation to care for offspring, but the underlying neuromolecular mechanisms have yet to be clarified. Here, we report that the calcitonin receptor (Calcr) and its ligand amylin are expressed in distinct neuronal populations in the medial preoptic area (MPOA) an...
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Veröffentlicht in: | Cell reports (Cambridge) 2021-06, Vol.35 (9), p.109204-109204, Article 109204 |
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creator | Yoshihara, Chihiro Tokita, Kenichi Maruyama, Teppo Kaneko, Misato Tsuneoka, Yousuke Fukumitsu, Kansai Miyazawa, Eri Shinozuka, Kazutaka Huang, Arthur J. Nishimori, Katsuhiko McHugh, Thomas J. Tanaka, Minoru Itohara, Shigeyoshi Touhara, Kazushige Miyamichi, Kazunari Kuroda, Kumi O. |
description | Maternal mammals exhibit heightened motivation to care for offspring, but the underlying neuromolecular mechanisms have yet to be clarified. Here, we report that the calcitonin receptor (Calcr) and its ligand amylin are expressed in distinct neuronal populations in the medial preoptic area (MPOA) and are upregulated in mothers. Calcr+ MPOA neurons activated by parental care project to somatomotor and monoaminergic brainstem nuclei. Retrograde monosynaptic tracing reveals that significant modification of afferents to Calcr+ neurons occurs in mothers. Knockdown of either Calcr or amylin gene expression hampers risk-taking maternal care, and specific silencing of Calcr+ MPOA neurons inhibits nurturing behaviors, while pharmacogenetic activation prevents infanticide in virgin males. These data indicate that Calcr+ MPOA neurons are required for both maternal and allomaternal nurturing behaviors and that upregulation of amylin-Calcr signaling in the MPOA at least partially mediates risk-taking maternal care, possibly via modified connectomics of Calcr+ neurons postpartum.
[Display omitted]
•Calcitonin receptor and its ligand amylin are expressed in the medial preoptic area•Calcitonin receptor + neurons are essential for maternal and alloparental care•Both calcitonin receptor and amylin are upregulated in postpartum mother mice•Calcitonin receptor upregulation takes part in risk-taking maternal behavior
Yoshihara et al. demonstrate that calcitonin receptor (Calcr)-expressing neurons in the central part of the medial preoptic area (cMPOA) are indispensable for both maternal and alloparental care in mice and that Calcr and its ligand amylin mediate heightened maternal motivation to care for young even under risky conditions. |
doi_str_mv | 10.1016/j.celrep.2021.109204 |
format | Article |
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[Display omitted]
•Calcitonin receptor and its ligand amylin are expressed in the medial preoptic area•Calcitonin receptor + neurons are essential for maternal and alloparental care•Both calcitonin receptor and amylin are upregulated in postpartum mother mice•Calcitonin receptor upregulation takes part in risk-taking maternal behavior
Yoshihara et al. demonstrate that calcitonin receptor (Calcr)-expressing neurons in the central part of the medial preoptic area (cMPOA) are indispensable for both maternal and alloparental care in mice and that Calcr and its ligand amylin mediate heightened maternal motivation to care for young even under risky conditions.</description><identifier>ISSN: 2211-1247</identifier><identifier>EISSN: 2211-1247</identifier><identifier>DOI: 10.1016/j.celrep.2021.109204</identifier><identifier>PMID: 34077719</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>amylin ; Animals ; Behavior, Animal - physiology ; calcitonin receptor ; central part of the medial preoptic area ; cMPOA ; Estrogens - metabolism ; Female ; Gene Silencing ; Gene Targeting ; Iapp ; infanticide ; islet amyloid poly-peptide ; Islet Amyloid Polypeptide - metabolism ; Lactation ; Ligands ; Male ; maternal behavior ; Maternal Behavior - physiology ; Mice ; Mice, Inbred C57BL ; Mus musculus ; Neurons - metabolism ; nurturing behavior ; parental behavior ; Postpartum Period ; Preoptic Area - metabolism ; Prolactin - metabolism ; Receptors, Calcitonin - metabolism ; Risk-Taking ; Signal Transduction ; Synapses - metabolism ; Up-Regulation</subject><ispartof>Cell reports (Cambridge), 2021-06, Vol.35 (9), p.109204-109204, Article 109204</ispartof><rights>2021 The Author(s)</rights><rights>Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c472t-eb71a9b8fe5bdb51d12f90a1d293536c037f6defdc38f8e55b5a627eb26916d83</citedby><cites>FETCH-LOGICAL-c472t-eb71a9b8fe5bdb51d12f90a1d293536c037f6defdc38f8e55b5a627eb26916d83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,864,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34077719$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yoshihara, Chihiro</creatorcontrib><creatorcontrib>Tokita, Kenichi</creatorcontrib><creatorcontrib>Maruyama, Teppo</creatorcontrib><creatorcontrib>Kaneko, Misato</creatorcontrib><creatorcontrib>Tsuneoka, Yousuke</creatorcontrib><creatorcontrib>Fukumitsu, Kansai</creatorcontrib><creatorcontrib>Miyazawa, Eri</creatorcontrib><creatorcontrib>Shinozuka, Kazutaka</creatorcontrib><creatorcontrib>Huang, Arthur J.</creatorcontrib><creatorcontrib>Nishimori, Katsuhiko</creatorcontrib><creatorcontrib>McHugh, Thomas J.</creatorcontrib><creatorcontrib>Tanaka, Minoru</creatorcontrib><creatorcontrib>Itohara, Shigeyoshi</creatorcontrib><creatorcontrib>Touhara, Kazushige</creatorcontrib><creatorcontrib>Miyamichi, Kazunari</creatorcontrib><creatorcontrib>Kuroda, Kumi O.</creatorcontrib><title>Calcitonin receptor signaling in the medial preoptic area enables risk-taking maternal care</title><title>Cell reports (Cambridge)</title><addtitle>Cell Rep</addtitle><description>Maternal mammals exhibit heightened motivation to care for offspring, but the underlying neuromolecular mechanisms have yet to be clarified. Here, we report that the calcitonin receptor (Calcr) and its ligand amylin are expressed in distinct neuronal populations in the medial preoptic area (MPOA) and are upregulated in mothers. Calcr+ MPOA neurons activated by parental care project to somatomotor and monoaminergic brainstem nuclei. Retrograde monosynaptic tracing reveals that significant modification of afferents to Calcr+ neurons occurs in mothers. Knockdown of either Calcr or amylin gene expression hampers risk-taking maternal care, and specific silencing of Calcr+ MPOA neurons inhibits nurturing behaviors, while pharmacogenetic activation prevents infanticide in virgin males. These data indicate that Calcr+ MPOA neurons are required for both maternal and allomaternal nurturing behaviors and that upregulation of amylin-Calcr signaling in the MPOA at least partially mediates risk-taking maternal care, possibly via modified connectomics of Calcr+ neurons postpartum.
[Display omitted]
•Calcitonin receptor and its ligand amylin are expressed in the medial preoptic area•Calcitonin receptor + neurons are essential for maternal and alloparental care•Both calcitonin receptor and amylin are upregulated in postpartum mother mice•Calcitonin receptor upregulation takes part in risk-taking maternal behavior
Yoshihara et al. demonstrate that calcitonin receptor (Calcr)-expressing neurons in the central part of the medial preoptic area (cMPOA) are indispensable for both maternal and alloparental care in mice and that Calcr and its ligand amylin mediate heightened maternal motivation to care for young even under risky conditions.</description><subject>amylin</subject><subject>Animals</subject><subject>Behavior, Animal - physiology</subject><subject>calcitonin receptor</subject><subject>central part of the medial preoptic area</subject><subject>cMPOA</subject><subject>Estrogens - metabolism</subject><subject>Female</subject><subject>Gene Silencing</subject><subject>Gene Targeting</subject><subject>Iapp</subject><subject>infanticide</subject><subject>islet amyloid poly-peptide</subject><subject>Islet Amyloid Polypeptide - metabolism</subject><subject>Lactation</subject><subject>Ligands</subject><subject>Male</subject><subject>maternal behavior</subject><subject>Maternal Behavior - physiology</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mus musculus</subject><subject>Neurons - metabolism</subject><subject>nurturing behavior</subject><subject>parental behavior</subject><subject>Postpartum Period</subject><subject>Preoptic Area - metabolism</subject><subject>Prolactin - metabolism</subject><subject>Receptors, Calcitonin - metabolism</subject><subject>Risk-Taking</subject><subject>Signal Transduction</subject><subject>Synapses - metabolism</subject><subject>Up-Regulation</subject><issn>2211-1247</issn><issn>2211-1247</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kE1LAzEQhoMoVmr_gUiOXrZmsh_ZvQhS_IKCFz15CEl2tqbd7q5JKvjvTdkqnpxLhuF5Z8hDyAWwOTAortdzg63DYc4ZhziqOMuOyBnnAAnwTBz_6Sdk5v2axSoYQJWdkkmaMSEEVGfkbaFaY0Pf2Y46NDiE3lFvV51qbbeicRrekW6xtqqlg8N-CNZQ5VBR7JRu0VNn_SYJarPntyqgi1lqInJOThrVepwd3il5vb97WTwmy-eHp8XtMjGZ4CFBLUBVumww17XOoQbeVExBzas0TwvDUtEUNTa1ScumxDzXuSq4QM2LCoq6TKfkatw7uP5jhz7IrfXRT6s67Hde8rilZIyLNKLZiBrXe--wkYOzW-W-JDC5NyvXcjQr92blaDbGLg8Xdjq6-A39eIzAzQhg_OenRSe9sdiZ6C1aDbLu7f8XvgHPvIwy</recordid><startdate>20210601</startdate><enddate>20210601</enddate><creator>Yoshihara, Chihiro</creator><creator>Tokita, Kenichi</creator><creator>Maruyama, Teppo</creator><creator>Kaneko, Misato</creator><creator>Tsuneoka, Yousuke</creator><creator>Fukumitsu, Kansai</creator><creator>Miyazawa, Eri</creator><creator>Shinozuka, Kazutaka</creator><creator>Huang, Arthur J.</creator><creator>Nishimori, Katsuhiko</creator><creator>McHugh, Thomas J.</creator><creator>Tanaka, Minoru</creator><creator>Itohara, Shigeyoshi</creator><creator>Touhara, Kazushige</creator><creator>Miyamichi, Kazunari</creator><creator>Kuroda, Kumi O.</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><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>7X8</scope></search><sort><creationdate>20210601</creationdate><title>Calcitonin receptor signaling in the medial preoptic area enables risk-taking maternal care</title><author>Yoshihara, Chihiro ; Tokita, Kenichi ; Maruyama, Teppo ; Kaneko, Misato ; Tsuneoka, Yousuke ; Fukumitsu, Kansai ; Miyazawa, Eri ; Shinozuka, Kazutaka ; Huang, Arthur J. ; Nishimori, Katsuhiko ; McHugh, Thomas J. ; Tanaka, Minoru ; Itohara, Shigeyoshi ; Touhara, Kazushige ; Miyamichi, Kazunari ; Kuroda, Kumi O.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c472t-eb71a9b8fe5bdb51d12f90a1d293536c037f6defdc38f8e55b5a627eb26916d83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>amylin</topic><topic>Animals</topic><topic>Behavior, Animal - physiology</topic><topic>calcitonin receptor</topic><topic>central part of the medial preoptic area</topic><topic>cMPOA</topic><topic>Estrogens - metabolism</topic><topic>Female</topic><topic>Gene Silencing</topic><topic>Gene Targeting</topic><topic>Iapp</topic><topic>infanticide</topic><topic>islet amyloid poly-peptide</topic><topic>Islet Amyloid Polypeptide - metabolism</topic><topic>Lactation</topic><topic>Ligands</topic><topic>Male</topic><topic>maternal behavior</topic><topic>Maternal Behavior - physiology</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mus musculus</topic><topic>Neurons - metabolism</topic><topic>nurturing behavior</topic><topic>parental behavior</topic><topic>Postpartum Period</topic><topic>Preoptic Area - metabolism</topic><topic>Prolactin - metabolism</topic><topic>Receptors, Calcitonin - metabolism</topic><topic>Risk-Taking</topic><topic>Signal Transduction</topic><topic>Synapses - metabolism</topic><topic>Up-Regulation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yoshihara, Chihiro</creatorcontrib><creatorcontrib>Tokita, Kenichi</creatorcontrib><creatorcontrib>Maruyama, Teppo</creatorcontrib><creatorcontrib>Kaneko, Misato</creatorcontrib><creatorcontrib>Tsuneoka, Yousuke</creatorcontrib><creatorcontrib>Fukumitsu, Kansai</creatorcontrib><creatorcontrib>Miyazawa, Eri</creatorcontrib><creatorcontrib>Shinozuka, Kazutaka</creatorcontrib><creatorcontrib>Huang, Arthur J.</creatorcontrib><creatorcontrib>Nishimori, Katsuhiko</creatorcontrib><creatorcontrib>McHugh, Thomas J.</creatorcontrib><creatorcontrib>Tanaka, Minoru</creatorcontrib><creatorcontrib>Itohara, Shigeyoshi</creatorcontrib><creatorcontrib>Touhara, Kazushige</creatorcontrib><creatorcontrib>Miyamichi, Kazunari</creatorcontrib><creatorcontrib>Kuroda, Kumi O.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Cell reports (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yoshihara, Chihiro</au><au>Tokita, Kenichi</au><au>Maruyama, Teppo</au><au>Kaneko, Misato</au><au>Tsuneoka, Yousuke</au><au>Fukumitsu, Kansai</au><au>Miyazawa, Eri</au><au>Shinozuka, Kazutaka</au><au>Huang, Arthur J.</au><au>Nishimori, Katsuhiko</au><au>McHugh, Thomas J.</au><au>Tanaka, Minoru</au><au>Itohara, Shigeyoshi</au><au>Touhara, Kazushige</au><au>Miyamichi, Kazunari</au><au>Kuroda, Kumi O.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Calcitonin receptor signaling in the medial preoptic area enables risk-taking maternal care</atitle><jtitle>Cell reports (Cambridge)</jtitle><addtitle>Cell Rep</addtitle><date>2021-06-01</date><risdate>2021</risdate><volume>35</volume><issue>9</issue><spage>109204</spage><epage>109204</epage><pages>109204-109204</pages><artnum>109204</artnum><issn>2211-1247</issn><eissn>2211-1247</eissn><abstract>Maternal mammals exhibit heightened motivation to care for offspring, but the underlying neuromolecular mechanisms have yet to be clarified. Here, we report that the calcitonin receptor (Calcr) and its ligand amylin are expressed in distinct neuronal populations in the medial preoptic area (MPOA) and are upregulated in mothers. Calcr+ MPOA neurons activated by parental care project to somatomotor and monoaminergic brainstem nuclei. Retrograde monosynaptic tracing reveals that significant modification of afferents to Calcr+ neurons occurs in mothers. Knockdown of either Calcr or amylin gene expression hampers risk-taking maternal care, and specific silencing of Calcr+ MPOA neurons inhibits nurturing behaviors, while pharmacogenetic activation prevents infanticide in virgin males. These data indicate that Calcr+ MPOA neurons are required for both maternal and allomaternal nurturing behaviors and that upregulation of amylin-Calcr signaling in the MPOA at least partially mediates risk-taking maternal care, possibly via modified connectomics of Calcr+ neurons postpartum.
[Display omitted]
•Calcitonin receptor and its ligand amylin are expressed in the medial preoptic area•Calcitonin receptor + neurons are essential for maternal and alloparental care•Both calcitonin receptor and amylin are upregulated in postpartum mother mice•Calcitonin receptor upregulation takes part in risk-taking maternal behavior
Yoshihara et al. demonstrate that calcitonin receptor (Calcr)-expressing neurons in the central part of the medial preoptic area (cMPOA) are indispensable for both maternal and alloparental care in mice and that Calcr and its ligand amylin mediate heightened maternal motivation to care for young even under risky conditions.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>34077719</pmid><doi>10.1016/j.celrep.2021.109204</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | amylin Animals Behavior, Animal - physiology calcitonin receptor central part of the medial preoptic area cMPOA Estrogens - metabolism Female Gene Silencing Gene Targeting Iapp infanticide islet amyloid poly-peptide Islet Amyloid Polypeptide - metabolism Lactation Ligands Male maternal behavior Maternal Behavior - physiology Mice Mice, Inbred C57BL Mus musculus Neurons - metabolism nurturing behavior parental behavior Postpartum Period Preoptic Area - metabolism Prolactin - metabolism Receptors, Calcitonin - metabolism Risk-Taking Signal Transduction Synapses - metabolism Up-Regulation |
title | Calcitonin receptor signaling in the medial preoptic area enables risk-taking maternal care |
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