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EIF4A3 deficient human iPSCs and mouse models demonstrate neural crest defects that underlie Richieri-Costa-Pereira syndrome
Biallelic loss-of-function mutations in the RNA-binding protein EIF4A3 cause Richieri-Costa-Pereira syndrome (RCPS), an autosomal recessive condition mainly characterized by craniofacial and limb malformations. However, the pathogenic cellular mechanisms responsible for this syndrome are entirely un...
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| Published in: | Human molecular genetics 2017-06, Vol.26 (12), p.2177-2191 |
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| creator | Miller, Emily E Kobayashi, Gerson S Musso, Camila M Allen, Miranda Ishiy, Felipe A A de Caires, Jr, Luiz Carlos Goulart, Ernesto Griesi-Oliveira, Karina Zechi-Ceide, Roseli M Richieri-Costa, Antonio Bertola, Debora R Passos-Bueno, Maria Rita Silver, Debra L |
| description | Biallelic loss-of-function mutations in the RNA-binding protein EIF4A3 cause Richieri-Costa-Pereira syndrome (RCPS), an autosomal recessive condition mainly characterized by craniofacial and limb malformations. However, the pathogenic cellular mechanisms responsible for this syndrome are entirely unknown. Here, we used two complementary approaches, patient-derived induced pluripotent stem cells (iPSCs) and conditional Eif4a3 mouse models, to demonstrate that defective neural crest cell (NCC) development explains RCPS craniofacial abnormalities. RCPS iNCCs have decreased migratory capacity, a distinct phenotype relative to other craniofacial disorders. Eif4a3 haploinsufficient embryos presented altered mandibular process fusion and micrognathia, thus recapitulating the most penetrant phenotypes of the syndrome. These defects were evident in either ubiquitous or NCC-specific Eif4a3 haploinsufficient animals, demonstrating an autonomous requirement of Eif4a3 in NCCs. Notably, RCPS NCC-derived mesenchymal stem-like cells (nMSCs) showed premature bone differentiation, a phenotype paralleled by premature clavicle ossification in Eif4a3 haploinsufficient embryos. Likewise, nMSCs presented compromised in vitro chondrogenesis, and Meckel's cartilage was underdeveloped in vivo. These findings indicate novel and essential requirements of EIF4A3 for NCC migration and osteochondrogenic differentiation during craniofacial development. Altogether, complementary use of iPSCs and mouse models pinpoint unique cellular mechanisms by which EIF4A3 mutation causes RCPS, and provide a paradigm to study craniofacial disorders. |
| doi_str_mv | 10.1093/hmg/ddx078 |
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However, the pathogenic cellular mechanisms responsible for this syndrome are entirely unknown. Here, we used two complementary approaches, patient-derived induced pluripotent stem cells (iPSCs) and conditional Eif4a3 mouse models, to demonstrate that defective neural crest cell (NCC) development explains RCPS craniofacial abnormalities. RCPS iNCCs have decreased migratory capacity, a distinct phenotype relative to other craniofacial disorders. Eif4a3 haploinsufficient embryos presented altered mandibular process fusion and micrognathia, thus recapitulating the most penetrant phenotypes of the syndrome. These defects were evident in either ubiquitous or NCC-specific Eif4a3 haploinsufficient animals, demonstrating an autonomous requirement of Eif4a3 in NCCs. Notably, RCPS NCC-derived mesenchymal stem-like cells (nMSCs) showed premature bone differentiation, a phenotype paralleled by premature clavicle ossification in Eif4a3 haploinsufficient embryos. Likewise, nMSCs presented compromised in vitro chondrogenesis, and Meckel's cartilage was underdeveloped in vivo. These findings indicate novel and essential requirements of EIF4A3 for NCC migration and osteochondrogenic differentiation during craniofacial development. Altogether, complementary use of iPSCs and mouse models pinpoint unique cellular mechanisms by which EIF4A3 mutation causes RCPS, and provide a paradigm to study craniofacial disorders.</description><identifier>ISSN: 0964-6906</identifier><identifier>EISSN: 1460-2083</identifier><identifier>DOI: 10.1093/hmg/ddx078</identifier><identifier>PMID: 28334780</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Animals ; Bone and Bones - metabolism ; Branchial Region - metabolism ; Cell Differentiation - genetics ; Cell Movement ; Chondrogenesis - genetics ; Clubfoot - genetics ; Clubfoot - metabolism ; Craniofacial Abnormalities - genetics ; Craniofacial Abnormalities - metabolism ; DEAD-box RNA Helicases - genetics ; DEAD-box RNA Helicases - metabolism ; Disease Models, Animal ; Eukaryotic Initiation Factor-4A - genetics ; Eukaryotic Initiation Factor-4A - metabolism ; Hand Deformities, Congenital - genetics ; Hand Deformities, Congenital - metabolism ; Humans ; Induced Pluripotent Stem Cells - metabolism ; Mice ; Neural Crest - growth & development ; Neural Crest - metabolism ; Osteogenesis - genetics ; Pierre Robin Syndrome - genetics ; Pierre Robin Syndrome - metabolism</subject><ispartof>Human molecular genetics, 2017-06, Vol.26 (12), p.2177-2191</ispartof><rights>The Author 2017. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com.</rights><rights>The Author 2017. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c378t-da77fdfca3c808ff1260527539ba71317b029b8ab71f1d63794235930449105f3</citedby><cites>FETCH-LOGICAL-c378t-da77fdfca3c808ff1260527539ba71317b029b8ab71f1d63794235930449105f3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,786,790,891,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28334780$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Miller, Emily E</creatorcontrib><creatorcontrib>Kobayashi, Gerson S</creatorcontrib><creatorcontrib>Musso, Camila M</creatorcontrib><creatorcontrib>Allen, Miranda</creatorcontrib><creatorcontrib>Ishiy, Felipe A A</creatorcontrib><creatorcontrib>de Caires, Jr, Luiz Carlos</creatorcontrib><creatorcontrib>Goulart, Ernesto</creatorcontrib><creatorcontrib>Griesi-Oliveira, Karina</creatorcontrib><creatorcontrib>Zechi-Ceide, Roseli M</creatorcontrib><creatorcontrib>Richieri-Costa, Antonio</creatorcontrib><creatorcontrib>Bertola, Debora R</creatorcontrib><creatorcontrib>Passos-Bueno, Maria Rita</creatorcontrib><creatorcontrib>Silver, Debra L</creatorcontrib><title>EIF4A3 deficient human iPSCs and mouse models demonstrate neural crest defects that underlie Richieri-Costa-Pereira syndrome</title><title>Human molecular genetics</title><addtitle>Hum Mol Genet</addtitle><description>Biallelic loss-of-function mutations in the RNA-binding protein EIF4A3 cause Richieri-Costa-Pereira syndrome (RCPS), an autosomal recessive condition mainly characterized by craniofacial and limb malformations. However, the pathogenic cellular mechanisms responsible for this syndrome are entirely unknown. Here, we used two complementary approaches, patient-derived induced pluripotent stem cells (iPSCs) and conditional Eif4a3 mouse models, to demonstrate that defective neural crest cell (NCC) development explains RCPS craniofacial abnormalities. RCPS iNCCs have decreased migratory capacity, a distinct phenotype relative to other craniofacial disorders. Eif4a3 haploinsufficient embryos presented altered mandibular process fusion and micrognathia, thus recapitulating the most penetrant phenotypes of the syndrome. These defects were evident in either ubiquitous or NCC-specific Eif4a3 haploinsufficient animals, demonstrating an autonomous requirement of Eif4a3 in NCCs. Notably, RCPS NCC-derived mesenchymal stem-like cells (nMSCs) showed premature bone differentiation, a phenotype paralleled by premature clavicle ossification in Eif4a3 haploinsufficient embryos. Likewise, nMSCs presented compromised in vitro chondrogenesis, and Meckel's cartilage was underdeveloped in vivo. These findings indicate novel and essential requirements of EIF4A3 for NCC migration and osteochondrogenic differentiation during craniofacial development. Altogether, complementary use of iPSCs and mouse models pinpoint unique cellular mechanisms by which EIF4A3 mutation causes RCPS, and provide a paradigm to study craniofacial disorders.</description><subject>Animals</subject><subject>Bone and Bones - metabolism</subject><subject>Branchial Region - metabolism</subject><subject>Cell Differentiation - genetics</subject><subject>Cell Movement</subject><subject>Chondrogenesis - genetics</subject><subject>Clubfoot - genetics</subject><subject>Clubfoot - metabolism</subject><subject>Craniofacial Abnormalities - genetics</subject><subject>Craniofacial Abnormalities - metabolism</subject><subject>DEAD-box RNA Helicases - genetics</subject><subject>DEAD-box RNA Helicases - metabolism</subject><subject>Disease Models, Animal</subject><subject>Eukaryotic Initiation Factor-4A - genetics</subject><subject>Eukaryotic Initiation Factor-4A - metabolism</subject><subject>Hand Deformities, Congenital - genetics</subject><subject>Hand Deformities, Congenital - metabolism</subject><subject>Humans</subject><subject>Induced Pluripotent Stem Cells - metabolism</subject><subject>Mice</subject><subject>Neural Crest - growth & development</subject><subject>Neural Crest - metabolism</subject><subject>Osteogenesis - genetics</subject><subject>Pierre Robin Syndrome - genetics</subject><subject>Pierre Robin Syndrome - metabolism</subject><issn>0964-6906</issn><issn>1460-2083</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNpVkUFrFTEUhYNY7OvTjT9AshRh7M0kM8lshPJoa6FgqboOmeROJzKTqUmmWOiPb8qrRTc3i_vl5JwcQt4z-Myg48fjfHPs3B-Q6hXZMNFCVYPir8kGulZUbQftITlK6RcAawWXb8hhrTgXUsGGPJxenIkTTh0O3noMmY7rbAL1V993iZrg6LysCct0OKWCzUtIOZqMNOAazURtxJSf7qPNiebRZLoGh3HySK-9HT1GX-2WlE11hRF9NDTdBxeXGd-Sg8FMCd89n1vy8-z0x-5rdfnt_GJ3cllZLlWunJFycIM13CpQw8DqFppaNrzrjWScyR7qrleml2xgruWyEzVvOg5CdAyagW_Jl73u7drP6GyJWZzr2-hnE-_1Yrz-fxP8qG-WO91IzkQR25KPzwJx-b2WvHr2yeI0mYDlezRTqpgSwKCgn_aojUtKEYeXZxjop7p0qUvv6yrwh3-NvaB_--GPok6TTw</recordid><startdate>20170615</startdate><enddate>20170615</enddate><creator>Miller, Emily E</creator><creator>Kobayashi, Gerson S</creator><creator>Musso, Camila M</creator><creator>Allen, Miranda</creator><creator>Ishiy, Felipe A A</creator><creator>de Caires, Jr, Luiz Carlos</creator><creator>Goulart, Ernesto</creator><creator>Griesi-Oliveira, Karina</creator><creator>Zechi-Ceide, Roseli M</creator><creator>Richieri-Costa, Antonio</creator><creator>Bertola, Debora R</creator><creator>Passos-Bueno, Maria Rita</creator><creator>Silver, Debra L</creator><general>Oxford University Press</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20170615</creationdate><title>EIF4A3 deficient human iPSCs and mouse models demonstrate neural crest defects that underlie Richieri-Costa-Pereira syndrome</title><author>Miller, Emily E ; Kobayashi, Gerson S ; Musso, Camila M ; Allen, Miranda ; Ishiy, Felipe A A ; de Caires, Jr, Luiz Carlos ; Goulart, Ernesto ; Griesi-Oliveira, Karina ; Zechi-Ceide, Roseli M ; Richieri-Costa, Antonio ; Bertola, Debora R ; Passos-Bueno, Maria Rita ; Silver, Debra L</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c378t-da77fdfca3c808ff1260527539ba71317b029b8ab71f1d63794235930449105f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Bone and Bones - metabolism</topic><topic>Branchial Region - metabolism</topic><topic>Cell Differentiation - genetics</topic><topic>Cell Movement</topic><topic>Chondrogenesis - genetics</topic><topic>Clubfoot - genetics</topic><topic>Clubfoot - metabolism</topic><topic>Craniofacial Abnormalities - genetics</topic><topic>Craniofacial Abnormalities - metabolism</topic><topic>DEAD-box RNA Helicases - genetics</topic><topic>DEAD-box RNA Helicases - metabolism</topic><topic>Disease Models, Animal</topic><topic>Eukaryotic Initiation Factor-4A - genetics</topic><topic>Eukaryotic Initiation Factor-4A - metabolism</topic><topic>Hand Deformities, Congenital - genetics</topic><topic>Hand Deformities, Congenital - metabolism</topic><topic>Humans</topic><topic>Induced Pluripotent Stem Cells - metabolism</topic><topic>Mice</topic><topic>Neural Crest - growth & development</topic><topic>Neural Crest - metabolism</topic><topic>Osteogenesis - genetics</topic><topic>Pierre Robin Syndrome - genetics</topic><topic>Pierre Robin Syndrome - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Miller, Emily E</creatorcontrib><creatorcontrib>Kobayashi, Gerson S</creatorcontrib><creatorcontrib>Musso, Camila M</creatorcontrib><creatorcontrib>Allen, Miranda</creatorcontrib><creatorcontrib>Ishiy, Felipe A A</creatorcontrib><creatorcontrib>de Caires, Jr, Luiz Carlos</creatorcontrib><creatorcontrib>Goulart, Ernesto</creatorcontrib><creatorcontrib>Griesi-Oliveira, Karina</creatorcontrib><creatorcontrib>Zechi-Ceide, Roseli M</creatorcontrib><creatorcontrib>Richieri-Costa, Antonio</creatorcontrib><creatorcontrib>Bertola, Debora R</creatorcontrib><creatorcontrib>Passos-Bueno, Maria Rita</creatorcontrib><creatorcontrib>Silver, Debra L</creatorcontrib><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><collection>PubMed Central (Full Participant titles)</collection><jtitle>Human molecular genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Miller, Emily E</au><au>Kobayashi, Gerson S</au><au>Musso, Camila M</au><au>Allen, Miranda</au><au>Ishiy, Felipe A A</au><au>de Caires, Jr, Luiz Carlos</au><au>Goulart, Ernesto</au><au>Griesi-Oliveira, Karina</au><au>Zechi-Ceide, Roseli M</au><au>Richieri-Costa, Antonio</au><au>Bertola, Debora R</au><au>Passos-Bueno, Maria Rita</au><au>Silver, Debra L</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>EIF4A3 deficient human iPSCs and mouse models demonstrate neural crest defects that underlie Richieri-Costa-Pereira syndrome</atitle><jtitle>Human molecular genetics</jtitle><addtitle>Hum Mol Genet</addtitle><date>2017-06-15</date><risdate>2017</risdate><volume>26</volume><issue>12</issue><spage>2177</spage><epage>2191</epage><pages>2177-2191</pages><issn>0964-6906</issn><eissn>1460-2083</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>Joint first authors.</notes><abstract>Biallelic loss-of-function mutations in the RNA-binding protein EIF4A3 cause Richieri-Costa-Pereira syndrome (RCPS), an autosomal recessive condition mainly characterized by craniofacial and limb malformations. However, the pathogenic cellular mechanisms responsible for this syndrome are entirely unknown. Here, we used two complementary approaches, patient-derived induced pluripotent stem cells (iPSCs) and conditional Eif4a3 mouse models, to demonstrate that defective neural crest cell (NCC) development explains RCPS craniofacial abnormalities. RCPS iNCCs have decreased migratory capacity, a distinct phenotype relative to other craniofacial disorders. Eif4a3 haploinsufficient embryos presented altered mandibular process fusion and micrognathia, thus recapitulating the most penetrant phenotypes of the syndrome. These defects were evident in either ubiquitous or NCC-specific Eif4a3 haploinsufficient animals, demonstrating an autonomous requirement of Eif4a3 in NCCs. Notably, RCPS NCC-derived mesenchymal stem-like cells (nMSCs) showed premature bone differentiation, a phenotype paralleled by premature clavicle ossification in Eif4a3 haploinsufficient embryos. Likewise, nMSCs presented compromised in vitro chondrogenesis, and Meckel's cartilage was underdeveloped in vivo. These findings indicate novel and essential requirements of EIF4A3 for NCC migration and osteochondrogenic differentiation during craniofacial development. Altogether, complementary use of iPSCs and mouse models pinpoint unique cellular mechanisms by which EIF4A3 mutation causes RCPS, and provide a paradigm to study craniofacial disorders.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>28334780</pmid><doi>10.1093/hmg/ddx078</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Bone and Bones - metabolism Branchial Region - metabolism Cell Differentiation - genetics Cell Movement Chondrogenesis - genetics Clubfoot - genetics Clubfoot - metabolism Craniofacial Abnormalities - genetics Craniofacial Abnormalities - metabolism DEAD-box RNA Helicases - genetics DEAD-box RNA Helicases - metabolism Disease Models, Animal Eukaryotic Initiation Factor-4A - genetics Eukaryotic Initiation Factor-4A - metabolism Hand Deformities, Congenital - genetics Hand Deformities, Congenital - metabolism Humans Induced Pluripotent Stem Cells - metabolism Mice Neural Crest - growth & development Neural Crest - metabolism Osteogenesis - genetics Pierre Robin Syndrome - genetics Pierre Robin Syndrome - metabolism |
| title | EIF4A3 deficient human iPSCs and mouse models demonstrate neural crest defects that underlie Richieri-Costa-Pereira syndrome |
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