Negative feedback loop of bone resorption by NFATc1-dependent induction of Cadm1
Trimethylation of histone H3 lysine 4 and lysine 27 (H3K4me3 and H3K27me3) at gene promoter regions critically regulates gene expression. Key developmental genes tend to exhibit changes in histone modification patterns from the H3K4me3/H3K27me3 bivalent pattern to the H3K4me3 monovalent pattern. Usi...
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| Veröffentlicht in: | PloS one 2017-04, Vol.12 (4), p.e0175632 |
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| creator | Nakamura, Shinya Koyama, Takuma Izawa, Naohiro Nomura, Seitaro Fujita, Takanori Omata, Yasunori Minami, Takashi Matsumoto, Morio Nakamura, Masaya Fujita-Jimbo, Eriko Momoi, Takashi Miyamoto, Takeshi Aburatani, Hiroyuki Tanaka, Sakae |
| description | Trimethylation of histone H3 lysine 4 and lysine 27 (H3K4me3 and H3K27me3) at gene promoter regions critically regulates gene expression. Key developmental genes tend to exhibit changes in histone modification patterns from the H3K4me3/H3K27me3 bivalent pattern to the H3K4me3 monovalent pattern. Using comprehensive chromatin immunoprecipitation followed by sequencing in bone marrow-derived macrophages (BMMs) and mature osteoclasts, we found that cell surface adhesion molecule 1 (Cadm1) is a direct target of nuclear factor of activated T cells 1 (NFATc1) and exhibits a bivalent histone pattern in BMMs and a monovalent pattern in osteoclasts. Cadm1 expression was upregulated in BMMs by receptor activator of nuclear factor kappa B ligand (RANKL), and blocked by a calcineurin/NFATc1 inhibitor, FK506. Cadm1-deficient mice exhibited significantly reduced bone mass compared with wild-type mice, which was due to the increased osteoclast differentiation, survival and bone-resorbing activity in Cadm1-deficient osteoclasts. These results suggest that Cadm1 is a direct target of NFATc1, which is induced by RANKL through epigenetic modification, and regulates osteoclastic bone resorption in a negative feedback manner. |
| doi_str_mv | 10.1371/journal.pone.0175632 |
| format | Article |
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Key developmental genes tend to exhibit changes in histone modification patterns from the H3K4me3/H3K27me3 bivalent pattern to the H3K4me3 monovalent pattern. Using comprehensive chromatin immunoprecipitation followed by sequencing in bone marrow-derived macrophages (BMMs) and mature osteoclasts, we found that cell surface adhesion molecule 1 (Cadm1) is a direct target of nuclear factor of activated T cells 1 (NFATc1) and exhibits a bivalent histone pattern in BMMs and a monovalent pattern in osteoclasts. Cadm1 expression was upregulated in BMMs by receptor activator of nuclear factor kappa B ligand (RANKL), and blocked by a calcineurin/NFATc1 inhibitor, FK506. Cadm1-deficient mice exhibited significantly reduced bone mass compared with wild-type mice, which was due to the increased osteoclast differentiation, survival and bone-resorbing activity in Cadm1-deficient osteoclasts. These results suggest that Cadm1 is a direct target of NFATc1, which is induced by RANKL through epigenetic modification, and regulates osteoclastic bone resorption in a negative feedback manner.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0175632</identifier><identifier>PMID: 28414795</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adapter proteins ; Animals ; Biology and Life Sciences ; Bone marrow ; Bone resorption ; Bone Resorption - genetics ; Bone Resorption - metabolism ; Bone Resorption - pathology ; Bone surgery ; Cell adhesion & migration ; Cell Adhesion Molecule-1 ; Cell Adhesion Molecules - biosynthesis ; Cell Adhesion Molecules - deficiency ; Cell Adhesion Molecules - genetics ; Cell Adhesion Molecules - metabolism ; Cell cycle ; Cell Differentiation ; Deoxyribonucleic acid ; DNA ; DNA methylation ; Epigenesis, Genetic ; Epigenetic inheritance ; Feedback, Physiological ; Gene Expression ; Genomes ; Histones - genetics ; Histones - metabolism ; Homeostasis ; Immune response ; Immune system ; Immunoglobulins - biosynthesis ; Immunoglobulins - deficiency ; Immunoglobulins - genetics ; Kinases ; Ligands ; Lung cancer ; Lymphocytes T ; Lysine ; Macrophages - cytology ; Macrophages - metabolism ; Male ; Medicine ; Medicine and Health Sciences ; Methylation ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Negative feedback ; NFATC Transcription Factors - metabolism ; Orthopedics ; Osteoclasts (Biology) ; Osteoclasts - cytology ; Osteoclasts - metabolism ; Polyclonal antibodies ; Promoter Regions, Genetic ; RANK Ligand - metabolism ; Research and Analysis Methods ; Science ; Stem cells ; T cells</subject><ispartof>PloS one, 2017-04, Vol.12 (4), p.e0175632</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Nakamura et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2017 Nakamura et al 2017 Nakamura et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-730368335d13cbc95295aba913df905cad9fa9d314802361c309eae070c34753</citedby><cites>FETCH-LOGICAL-c692t-730368335d13cbc95295aba913df905cad9fa9d314802361c309eae070c34753</cites><orcidid>0000-0001-9373-5142</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5393607/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5393607/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28414795$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Reddy, Sakamuri V.</contributor><creatorcontrib>Nakamura, Shinya</creatorcontrib><creatorcontrib>Koyama, Takuma</creatorcontrib><creatorcontrib>Izawa, Naohiro</creatorcontrib><creatorcontrib>Nomura, Seitaro</creatorcontrib><creatorcontrib>Fujita, Takanori</creatorcontrib><creatorcontrib>Omata, Yasunori</creatorcontrib><creatorcontrib>Minami, Takashi</creatorcontrib><creatorcontrib>Matsumoto, Morio</creatorcontrib><creatorcontrib>Nakamura, Masaya</creatorcontrib><creatorcontrib>Fujita-Jimbo, Eriko</creatorcontrib><creatorcontrib>Momoi, Takashi</creatorcontrib><creatorcontrib>Miyamoto, Takeshi</creatorcontrib><creatorcontrib>Aburatani, Hiroyuki</creatorcontrib><creatorcontrib>Tanaka, Sakae</creatorcontrib><title>Negative feedback loop of bone resorption by NFATc1-dependent induction of Cadm1</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Trimethylation of histone H3 lysine 4 and lysine 27 (H3K4me3 and H3K27me3) at gene promoter regions critically regulates gene expression. Key developmental genes tend to exhibit changes in histone modification patterns from the H3K4me3/H3K27me3 bivalent pattern to the H3K4me3 monovalent pattern. Using comprehensive chromatin immunoprecipitation followed by sequencing in bone marrow-derived macrophages (BMMs) and mature osteoclasts, we found that cell surface adhesion molecule 1 (Cadm1) is a direct target of nuclear factor of activated T cells 1 (NFATc1) and exhibits a bivalent histone pattern in BMMs and a monovalent pattern in osteoclasts. Cadm1 expression was upregulated in BMMs by receptor activator of nuclear factor kappa B ligand (RANKL), and blocked by a calcineurin/NFATc1 inhibitor, FK506. Cadm1-deficient mice exhibited significantly reduced bone mass compared with wild-type mice, which was due to the increased osteoclast differentiation, survival and bone-resorbing activity in Cadm1-deficient osteoclasts. These results suggest that Cadm1 is a direct target of NFATc1, which is induced by RANKL through epigenetic modification, and regulates osteoclastic bone resorption in a negative feedback manner.</description><subject>Adapter proteins</subject><subject>Animals</subject><subject>Biology and Life Sciences</subject><subject>Bone marrow</subject><subject>Bone resorption</subject><subject>Bone Resorption - genetics</subject><subject>Bone Resorption - metabolism</subject><subject>Bone Resorption - pathology</subject><subject>Bone surgery</subject><subject>Cell adhesion & migration</subject><subject>Cell Adhesion Molecule-1</subject><subject>Cell Adhesion Molecules - biosynthesis</subject><subject>Cell Adhesion Molecules - deficiency</subject><subject>Cell Adhesion Molecules - genetics</subject><subject>Cell Adhesion Molecules - metabolism</subject><subject>Cell cycle</subject><subject>Cell Differentiation</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>Epigenesis, Genetic</subject><subject>Epigenetic inheritance</subject><subject>Feedback, Physiological</subject><subject>Gene Expression</subject><subject>Genomes</subject><subject>Histones - genetics</subject><subject>Histones - metabolism</subject><subject>Homeostasis</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunoglobulins - biosynthesis</subject><subject>Immunoglobulins - deficiency</subject><subject>Immunoglobulins - genetics</subject><subject>Kinases</subject><subject>Ligands</subject><subject>Lung cancer</subject><subject>Lymphocytes T</subject><subject>Lysine</subject><subject>Macrophages - cytology</subject><subject>Macrophages - metabolism</subject><subject>Male</subject><subject>Medicine</subject><subject>Medicine and Health Sciences</subject><subject>Methylation</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Negative feedback</subject><subject>NFATC Transcription Factors - metabolism</subject><subject>Orthopedics</subject><subject>Osteoclasts (Biology)</subject><subject>Osteoclasts - cytology</subject><subject>Osteoclasts - metabolism</subject><subject>Polyclonal antibodies</subject><subject>Promoter Regions, Genetic</subject><subject>RANK Ligand - metabolism</subject><subject>Research and Analysis Methods</subject><subject>Science</subject><subject>Stem cells</subject><subject>T cells</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNkl1v0zAUhiMEYmPwDxBEQkJw0eKPxB83SFW1QaVpQ1Bxazn2SeuSxlmcTNu_x22zqUG7QL6wZT_va5_jN0neYjTFlOMvG9-3ta6mja9hijDPGSXPklMsKZkwgujzo_VJ8iqEDUI5FYy9TE6IyHDGZX6a_LiCle7cLaQlgC20-ZNW3jepL9MiGqctBN82nfN1WtynVxezpcETCw3UFuoudbXtzf40CubabvHr5EWpqwBvhvksWV6cL-ffJ5fX3xbz2eXEMEm6CaeIMkFpbjE1hZE5kbkutMTUlhLlRltZamkpzgQilGFDkQQNiCNDM57Ts-T9wbapfFBDL4LCQgiZ8YzsiMWBsF5vVNO6rW7vlddO7Td8u1K67ZypQJEc0bzkQgpGMoal4AJbS6QusADQInp9HW7riy1YE0tvdTUyHZ_Ubq1W_lblVFKGeDT4NBi0_qaH0KmtCwaqStfg-_27JRUZJyyiH_5Bn65uoFY6FuDq0sd7zc5UzbJYCGGMyUhNn6DisLB1Jv5v6eL-SPB5JIhMB3fdSvchqMWvn__PXv8esx-P2DXoqlsHX_W76IQxmB1A0_oQWigfm4yR2uX-oRtql3s15D7K3h1_0KPoIej0LzNc-sI</recordid><startdate>20170417</startdate><enddate>20170417</enddate><creator>Nakamura, Shinya</creator><creator>Koyama, Takuma</creator><creator>Izawa, Naohiro</creator><creator>Nomura, Seitaro</creator><creator>Fujita, Takanori</creator><creator>Omata, Yasunori</creator><creator>Minami, Takashi</creator><creator>Matsumoto, Morio</creator><creator>Nakamura, Masaya</creator><creator>Fujita-Jimbo, Eriko</creator><creator>Momoi, Takashi</creator><creator>Miyamoto, Takeshi</creator><creator>Aburatani, Hiroyuki</creator><creator>Tanaka, Sakae</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-9373-5142</orcidid></search><sort><creationdate>20170417</creationdate><title>Negative feedback loop of bone resorption by NFATc1-dependent induction of Cadm1</title><author>Nakamura, Shinya ; Koyama, Takuma ; Izawa, Naohiro ; Nomura, Seitaro ; Fujita, Takanori ; Omata, Yasunori ; Minami, Takashi ; Matsumoto, Morio ; Nakamura, Masaya ; Fujita-Jimbo, Eriko ; Momoi, Takashi ; Miyamoto, Takeshi ; Aburatani, Hiroyuki ; Tanaka, Sakae</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-730368335d13cbc95295aba913df905cad9fa9d314802361c309eae070c34753</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Adapter proteins</topic><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Bone marrow</topic><topic>Bone resorption</topic><topic>Bone Resorption - genetics</topic><topic>Bone Resorption - metabolism</topic><topic>Bone Resorption - pathology</topic><topic>Bone surgery</topic><topic>Cell adhesion & migration</topic><topic>Cell Adhesion Molecule-1</topic><topic>Cell Adhesion Molecules - biosynthesis</topic><topic>Cell Adhesion Molecules - deficiency</topic><topic>Cell Adhesion Molecules - genetics</topic><topic>Cell Adhesion Molecules - metabolism</topic><topic>Cell cycle</topic><topic>Cell Differentiation</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA methylation</topic><topic>Epigenesis, Genetic</topic><topic>Epigenetic inheritance</topic><topic>Feedback, Physiological</topic><topic>Gene Expression</topic><topic>Genomes</topic><topic>Histones - genetics</topic><topic>Histones - metabolism</topic><topic>Homeostasis</topic><topic>Immune response</topic><topic>Immune system</topic><topic>Immunoglobulins - biosynthesis</topic><topic>Immunoglobulins - deficiency</topic><topic>Immunoglobulins - genetics</topic><topic>Kinases</topic><topic>Ligands</topic><topic>Lung cancer</topic><topic>Lymphocytes T</topic><topic>Lysine</topic><topic>Macrophages - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nakamura, Shinya</au><au>Koyama, Takuma</au><au>Izawa, Naohiro</au><au>Nomura, Seitaro</au><au>Fujita, Takanori</au><au>Omata, Yasunori</au><au>Minami, Takashi</au><au>Matsumoto, Morio</au><au>Nakamura, Masaya</au><au>Fujita-Jimbo, Eriko</au><au>Momoi, Takashi</au><au>Miyamoto, Takeshi</au><au>Aburatani, Hiroyuki</au><au>Tanaka, Sakae</au><au>Reddy, Sakamuri V.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Negative feedback loop of bone resorption by NFATc1-dependent induction of Cadm1</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-04-17</date><risdate>2017</risdate><volume>12</volume><issue>4</issue><spage>e0175632</spage><pages>e0175632-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Trimethylation of histone H3 lysine 4 and lysine 27 (H3K4me3 and H3K27me3) at gene promoter regions critically regulates gene expression. Key developmental genes tend to exhibit changes in histone modification patterns from the H3K4me3/H3K27me3 bivalent pattern to the H3K4me3 monovalent pattern. Using comprehensive chromatin immunoprecipitation followed by sequencing in bone marrow-derived macrophages (BMMs) and mature osteoclasts, we found that cell surface adhesion molecule 1 (Cadm1) is a direct target of nuclear factor of activated T cells 1 (NFATc1) and exhibits a bivalent histone pattern in BMMs and a monovalent pattern in osteoclasts. Cadm1 expression was upregulated in BMMs by receptor activator of nuclear factor kappa B ligand (RANKL), and blocked by a calcineurin/NFATc1 inhibitor, FK506. Cadm1-deficient mice exhibited significantly reduced bone mass compared with wild-type mice, which was due to the increased osteoclast differentiation, survival and bone-resorbing activity in Cadm1-deficient osteoclasts. These results suggest that Cadm1 is a direct target of NFATc1, which is induced by RANKL through epigenetic modification, and regulates osteoclastic bone resorption in a negative feedback manner.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28414795</pmid><doi>10.1371/journal.pone.0175632</doi><tpages>e0175632</tpages><orcidid>https://orcid.org/0000-0001-9373-5142</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2017-04, Vol.12 (4), p.e0175632 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1888947425 |
| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adapter proteins Animals Biology and Life Sciences Bone marrow Bone resorption Bone Resorption - genetics Bone Resorption - metabolism Bone Resorption - pathology Bone surgery Cell adhesion & migration Cell Adhesion Molecule-1 Cell Adhesion Molecules - biosynthesis Cell Adhesion Molecules - deficiency Cell Adhesion Molecules - genetics Cell Adhesion Molecules - metabolism Cell cycle Cell Differentiation Deoxyribonucleic acid DNA DNA methylation Epigenesis, Genetic Epigenetic inheritance Feedback, Physiological Gene Expression Genomes Histones - genetics Histones - metabolism Homeostasis Immune response Immune system Immunoglobulins - biosynthesis Immunoglobulins - deficiency Immunoglobulins - genetics Kinases Ligands Lung cancer Lymphocytes T Lysine Macrophages - cytology Macrophages - metabolism Male Medicine Medicine and Health Sciences Methylation Mice Mice, Inbred C57BL Mice, Knockout Negative feedback NFATC Transcription Factors - metabolism Orthopedics Osteoclasts (Biology) Osteoclasts - cytology Osteoclasts - metabolism Polyclonal antibodies Promoter Regions, Genetic RANK Ligand - metabolism Research and Analysis Methods Science Stem cells T cells |
| title | Negative feedback loop of bone resorption by NFATc1-dependent induction of Cadm1 |
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