An evolutionarily acquired microRNA shapes development of mammalian cortical projections
The corticospinal tract is unique to mammals and the corpus callosum is unique to placental mammals (eutherians). The emergence of these structures is thought to underpin the evolutionary acquisition of complex motor and cognitive skills. Corticospinal motor neurons (CSMN) and callosal projection ne...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2020-11, Vol.117 (46), p.29113-29122 |
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| creator | Diaz, Jessica L. Siththanandan, Verl B. Lu, Victoria Gonzalez-Nava, Nicole Pasquina, Lincoln MacDonald, Jessica L. Woodworth, Mollie B. Ozkan, Abdulkadir Nair, Ramesh He, Zihuai Sahni, Vibhu Sarnow, Peter Palmer, Theo D. Macklis, Jeffrey D. Tharin, Suzanne |
| description | The corticospinal tract is unique to mammals and the corpus callosum is unique to placental mammals (eutherians). The emergence of these structures is thought to underpin the evolutionary acquisition of complex motor and cognitive skills. Corticospinal motor neurons (CSMN) and callosal projection neurons (CPN) are the archetypal projection neurons of the corticospinal tract and corpus callosum, respectively. Although a number of conserved transcriptional regulators of CSMN and CPN development have been identified in vertebrates, none are unique to mammals and most are coexpressed across multiple projection neuron subtypes. Here, we discover 17 CSMN-enriched microRNAs (miRNAs), 15 of which map to a single genomic cluster that is exclusive to eutherians. One of these, miR-409-3p, promotes CSMN subtype identity in part via repression of LMO4, a key transcriptional regulator of CPN development. In vivo, miR-409-3p is sufficient to convert deep-layer CPN into CSMN. This is a demonstration of an evolutionarily acquired miRNA in eutherians that refines cortical projection neuron subtype development. Our findings implicate miRNAs in the eutherians’ increase in neuronal subtype and projection diversity, the anatomic underpinnings of their complex behavior. |
| doi_str_mv | 10.1073/pnas.2006700117 |
| format | Article |
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The emergence of these structures is thought to underpin the evolutionary acquisition of complex motor and cognitive skills. Corticospinal motor neurons (CSMN) and callosal projection neurons (CPN) are the archetypal projection neurons of the corticospinal tract and corpus callosum, respectively. Although a number of conserved transcriptional regulators of CSMN and CPN development have been identified in vertebrates, none are unique to mammals and most are coexpressed across multiple projection neuron subtypes. Here, we discover 17 CSMN-enriched microRNAs (miRNAs), 15 of which map to a single genomic cluster that is exclusive to eutherians. One of these, miR-409-3p, promotes CSMN subtype identity in part via repression of LMO4, a key transcriptional regulator of CPN development. In vivo, miR-409-3p is sufficient to convert deep-layer CPN into CSMN. This is a demonstration of an evolutionarily acquired miRNA in eutherians that refines cortical projection neuron subtype development. Our findings implicate miRNAs in the eutherians’ increase in neuronal subtype and projection diversity, the anatomic underpinnings of their complex behavior.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2006700117</identifier><identifier>PMID: 33139574</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Biological Evolution ; Biological Sciences ; Cerebral Cortex - physiology ; Cognition & reasoning ; Cognitive ability ; Corpus callosum ; Corpus Callosum - physiology ; Eutheria - genetics ; Evolution ; Gene Expression Regulation, Developmental ; Mammals ; Mammals - genetics ; Mice ; MicroRNAs ; MicroRNAs - genetics ; MicroRNAs - physiology ; miRNA ; Motor Cortex - pathology ; Motor Neurons ; Motor skill ; Neurons ; Projection ; Pyramidal tracts ; Pyramidal Tracts - pathology ; Regulators ; Ribonucleic acid ; RNA ; Transcription ; Vertebrates</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2020-11, Vol.117 (46), p.29113-29122</ispartof><rights>Copyright © 2020 the Author(s). Published by PNAS.</rights><rights>Copyright National Academy of Sciences Nov 17, 2020</rights><rights>Copyright © 2020 the Author(s). Published by PNAS. 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c443t-f54ee2a25440ffca4b16c5c1947da1b603bf60f58c8c01de97276db393f298eb3</citedby><cites>FETCH-LOGICAL-c443t-f54ee2a25440ffca4b16c5c1947da1b603bf60f58c8c01de97276db393f298eb3</cites><orcidid>0000-0001-8005-4348 ; 0000-0002-9111-5756 ; 0000-0002-1323-3247 ; 0000-0003-2130-2289 ; 0000-0002-8040-1191 ; 0000-0003-2499-7637 ; 0000-0001-8584-6766 ; 0000-0002-2043-2770</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26971036$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26971036$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33139574$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Diaz, Jessica L.</creatorcontrib><creatorcontrib>Siththanandan, Verl B.</creatorcontrib><creatorcontrib>Lu, Victoria</creatorcontrib><creatorcontrib>Gonzalez-Nava, Nicole</creatorcontrib><creatorcontrib>Pasquina, Lincoln</creatorcontrib><creatorcontrib>MacDonald, Jessica L.</creatorcontrib><creatorcontrib>Woodworth, Mollie B.</creatorcontrib><creatorcontrib>Ozkan, Abdulkadir</creatorcontrib><creatorcontrib>Nair, Ramesh</creatorcontrib><creatorcontrib>He, Zihuai</creatorcontrib><creatorcontrib>Sahni, Vibhu</creatorcontrib><creatorcontrib>Sarnow, Peter</creatorcontrib><creatorcontrib>Palmer, Theo D.</creatorcontrib><creatorcontrib>Macklis, Jeffrey D.</creatorcontrib><creatorcontrib>Tharin, Suzanne</creatorcontrib><title>An evolutionarily acquired microRNA shapes development of mammalian cortical projections</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The corticospinal tract is unique to mammals and the corpus callosum is unique to placental mammals (eutherians). The emergence of these structures is thought to underpin the evolutionary acquisition of complex motor and cognitive skills. Corticospinal motor neurons (CSMN) and callosal projection neurons (CPN) are the archetypal projection neurons of the corticospinal tract and corpus callosum, respectively. Although a number of conserved transcriptional regulators of CSMN and CPN development have been identified in vertebrates, none are unique to mammals and most are coexpressed across multiple projection neuron subtypes. Here, we discover 17 CSMN-enriched microRNAs (miRNAs), 15 of which map to a single genomic cluster that is exclusive to eutherians. One of these, miR-409-3p, promotes CSMN subtype identity in part via repression of LMO4, a key transcriptional regulator of CPN development. In vivo, miR-409-3p is sufficient to convert deep-layer CPN into CSMN. This is a demonstration of an evolutionarily acquired miRNA in eutherians that refines cortical projection neuron subtype development. Our findings implicate miRNAs in the eutherians’ increase in neuronal subtype and projection diversity, the anatomic underpinnings of their complex behavior.</description><subject>Animals</subject><subject>Biological Evolution</subject><subject>Biological Sciences</subject><subject>Cerebral Cortex - physiology</subject><subject>Cognition & reasoning</subject><subject>Cognitive ability</subject><subject>Corpus callosum</subject><subject>Corpus Callosum - physiology</subject><subject>Eutheria - genetics</subject><subject>Evolution</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Mammals</subject><subject>Mammals - genetics</subject><subject>Mice</subject><subject>MicroRNAs</subject><subject>MicroRNAs - genetics</subject><subject>MicroRNAs - physiology</subject><subject>miRNA</subject><subject>Motor Cortex - pathology</subject><subject>Motor Neurons</subject><subject>Motor skill</subject><subject>Neurons</subject><subject>Projection</subject><subject>Pyramidal tracts</subject><subject>Pyramidal Tracts - pathology</subject><subject>Regulators</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Transcription</subject><subject>Vertebrates</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkUuLFDEUhYMoTju6dqUUzMZNzdy8k43QDL5gUBAFdyGVSpw0VZWapKph_r1pemwfq7s43z2cew9CLzFcYpD0ap5suSQAQgJgLB-hDQaNW8E0PEYbACJbxQg7Q89K2QGA5gqeojNKMdVcsg36sZ0av0_DusQ02RyH-8a6uzVm3zdjdDl9_bxtyq2dfWl6v_dDmkc_LU0KzWjH0Q7RTo1LeYnODs2c0867g1V5jp4EOxT_4mGeo-_v3327_tjefPnw6Xp70zrG6NIGzrwnlnDGIARnWYeF4w5rJnuLOwG0CwICV045wL3XkkjRd1TTQLTyHT1Hb4--89qNvnc1XLaDmXMcbb43yUbzrzLFW_Mz7Y0UilCiqsGbB4Oc7lZfFjPG4vww2MmntRjCuKTAuOIVvfgP3aU1T_W8SgmmBGNcV-rqSNXvlZJ9OIXBYA6tmUNr5k9rdeP13zec-N81VeDVEdiVJeWTToSWGKigvwCHhJ8h</recordid><startdate>20201117</startdate><enddate>20201117</enddate><creator>Diaz, Jessica L.</creator><creator>Siththanandan, Verl B.</creator><creator>Lu, Victoria</creator><creator>Gonzalez-Nava, Nicole</creator><creator>Pasquina, Lincoln</creator><creator>MacDonald, Jessica L.</creator><creator>Woodworth, Mollie B.</creator><creator>Ozkan, Abdulkadir</creator><creator>Nair, Ramesh</creator><creator>He, Zihuai</creator><creator>Sahni, Vibhu</creator><creator>Sarnow, Peter</creator><creator>Palmer, Theo D.</creator><creator>Macklis, Jeffrey D.</creator><creator>Tharin, Suzanne</creator><general>National Academy of Sciences</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8005-4348</orcidid><orcidid>https://orcid.org/0000-0002-9111-5756</orcidid><orcidid>https://orcid.org/0000-0002-1323-3247</orcidid><orcidid>https://orcid.org/0000-0003-2130-2289</orcidid><orcidid>https://orcid.org/0000-0002-8040-1191</orcidid><orcidid>https://orcid.org/0000-0003-2499-7637</orcidid><orcidid>https://orcid.org/0000-0001-8584-6766</orcidid><orcidid>https://orcid.org/0000-0002-2043-2770</orcidid></search><sort><creationdate>20201117</creationdate><title>An evolutionarily acquired microRNA shapes development of mammalian cortical projections</title><author>Diaz, Jessica L. ; 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The emergence of these structures is thought to underpin the evolutionary acquisition of complex motor and cognitive skills. Corticospinal motor neurons (CSMN) and callosal projection neurons (CPN) are the archetypal projection neurons of the corticospinal tract and corpus callosum, respectively. Although a number of conserved transcriptional regulators of CSMN and CPN development have been identified in vertebrates, none are unique to mammals and most are coexpressed across multiple projection neuron subtypes. Here, we discover 17 CSMN-enriched microRNAs (miRNAs), 15 of which map to a single genomic cluster that is exclusive to eutherians. One of these, miR-409-3p, promotes CSMN subtype identity in part via repression of LMO4, a key transcriptional regulator of CPN development. In vivo, miR-409-3p is sufficient to convert deep-layer CPN into CSMN. This is a demonstration of an evolutionarily acquired miRNA in eutherians that refines cortical projection neuron subtype development. Our findings implicate miRNAs in the eutherians’ increase in neuronal subtype and projection diversity, the anatomic underpinnings of their complex behavior.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>33139574</pmid><doi>10.1073/pnas.2006700117</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-8005-4348</orcidid><orcidid>https://orcid.org/0000-0002-9111-5756</orcidid><orcidid>https://orcid.org/0000-0002-1323-3247</orcidid><orcidid>https://orcid.org/0000-0003-2130-2289</orcidid><orcidid>https://orcid.org/0000-0002-8040-1191</orcidid><orcidid>https://orcid.org/0000-0003-2499-7637</orcidid><orcidid>https://orcid.org/0000-0001-8584-6766</orcidid><orcidid>https://orcid.org/0000-0002-2043-2770</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biological Evolution Biological Sciences Cerebral Cortex - physiology Cognition & reasoning Cognitive ability Corpus callosum Corpus Callosum - physiology Eutheria - genetics Evolution Gene Expression Regulation, Developmental Mammals Mammals - genetics Mice MicroRNAs MicroRNAs - genetics MicroRNAs - physiology miRNA Motor Cortex - pathology Motor Neurons Motor skill Neurons Projection Pyramidal tracts Pyramidal Tracts - pathology Regulators Ribonucleic acid RNA Transcription Vertebrates |
| title | An evolutionarily acquired microRNA shapes development of mammalian cortical projections |
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