Disruption of PHF21A causes syndromic intellectual disability with craniofacial anomalies, epilepsy, hypotonia, and neurobehavioral problems including autism

<h3>Background</h3><p dir="ltr">PHF21A has been associated with intellectual disability and craniofacial anomalies based on its deletion in the Potocki-Shaffer syndrome region at 11p11.2 and its disruption in three patients with balanced translocations. In addition, three...

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Main Author: Hyung-Goo Kim (728597) (author)
Other Authors: Jill A. Rosenfeld (9606199) (author), Daryl A. Scott (10139232) (author), Gerard Bénédicte (18615115) (author), Jonathan D. Labonne (18615118) (author), Jason Brown (253739) (author), Marianne McGuire (4355386) (author), Sonal Mahida (6413285) (author), Sakkubai Naidu (804374) (author), Jacqueline Gutierrez (7532777) (author), Gaetan Lesca (6380633) (author), Vincent des Portes (449415) (author), Ange-Line Bruel (3178743) (author), Arthur Sorlin (7532780) (author), Fan Xia (219575) (author), Yline Capri (3181152) (author), Eric Muller (2212156) (author), Dianalee McKnight (7532783) (author), Erin Torti (7532786) (author), Franz Rüschendorf (73756) (author), Oliver Hummel (30411) (author), Zeyaul Islam (5867387) (author), Prasanna R. Kolatkar (124118) (author), Lawrence C. Layman (13913559) (author), Duchwan Ryu (7532795) (author), Il-Keun Kong (85884) (author), Suneeta Madan-Khetarpal (4355359) (author), Cheol-Hee Kim (36752) (author)
Published: 2019
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_version_ 1864513514054352896
author Hyung-Goo Kim (728597)
author2 Jill A. Rosenfeld (9606199)
Daryl A. Scott (10139232)
Gerard Bénédicte (18615115)
Jonathan D. Labonne (18615118)
Jason Brown (253739)
Marianne McGuire (4355386)
Sonal Mahida (6413285)
Sakkubai Naidu (804374)
Jacqueline Gutierrez (7532777)
Gaetan Lesca (6380633)
Vincent des Portes (449415)
Ange-Line Bruel (3178743)
Arthur Sorlin (7532780)
Fan Xia (219575)
Yline Capri (3181152)
Eric Muller (2212156)
Dianalee McKnight (7532783)
Erin Torti (7532786)
Franz Rüschendorf (73756)
Oliver Hummel (30411)
Zeyaul Islam (5867387)
Prasanna R. Kolatkar (124118)
Lawrence C. Layman (13913559)
Duchwan Ryu (7532795)
Il-Keun Kong (85884)
Suneeta Madan-Khetarpal (4355359)
Cheol-Hee Kim (36752)
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
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author
author_facet Hyung-Goo Kim (728597)
Jill A. Rosenfeld (9606199)
Daryl A. Scott (10139232)
Gerard Bénédicte (18615115)
Jonathan D. Labonne (18615118)
Jason Brown (253739)
Marianne McGuire (4355386)
Sonal Mahida (6413285)
Sakkubai Naidu (804374)
Jacqueline Gutierrez (7532777)
Gaetan Lesca (6380633)
Vincent des Portes (449415)
Ange-Line Bruel (3178743)
Arthur Sorlin (7532780)
Fan Xia (219575)
Yline Capri (3181152)
Eric Muller (2212156)
Dianalee McKnight (7532783)
Erin Torti (7532786)
Franz Rüschendorf (73756)
Oliver Hummel (30411)
Zeyaul Islam (5867387)
Prasanna R. Kolatkar (124118)
Lawrence C. Layman (13913559)
Duchwan Ryu (7532795)
Il-Keun Kong (85884)
Suneeta Madan-Khetarpal (4355359)
Cheol-Hee Kim (36752)
author_role author
dc.creator.none.fl_str_mv Hyung-Goo Kim (728597)
Jill A. Rosenfeld (9606199)
Daryl A. Scott (10139232)
Gerard Bénédicte (18615115)
Jonathan D. Labonne (18615118)
Jason Brown (253739)
Marianne McGuire (4355386)
Sonal Mahida (6413285)
Sakkubai Naidu (804374)
Jacqueline Gutierrez (7532777)
Gaetan Lesca (6380633)
Vincent des Portes (449415)
Ange-Line Bruel (3178743)
Arthur Sorlin (7532780)
Fan Xia (219575)
Yline Capri (3181152)
Eric Muller (2212156)
Dianalee McKnight (7532783)
Erin Torti (7532786)
Franz Rüschendorf (73756)
Oliver Hummel (30411)
Zeyaul Islam (5867387)
Prasanna R. Kolatkar (124118)
Lawrence C. Layman (13913559)
Duchwan Ryu (7532795)
Il-Keun Kong (85884)
Suneeta Madan-Khetarpal (4355359)
Cheol-Hee Kim (36752)
dc.date.none.fl_str_mv 2019-10-22T03:00:00Z
dc.identifier.none.fl_str_mv 10.1186/s13229-019-0286-0
dc.relation.none.fl_str_mv https://figshare.com/articles/journal_contribution/Disruption_of_PHF21A_causes_syndromic_intellectual_disability_with_craniofacial_anomalies_epilepsy_hypotonia_and_neurobehavioral_problems_including_autism/25904413
dc.rights.none.fl_str_mv CC BY 4.0
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Biological sciences
Genetics
PHF21A
BHC80
Intellectual disability (ID)
Autism spectrum disorder (ASD)
Neurodevelopmental disorders
Potocki-Shaffer syndrome (PSS)
AT Hook domain
Intrinsically disordered region (IDR)
KDM1A
dc.title.none.fl_str_mv Disruption of PHF21A causes syndromic intellectual disability with craniofacial anomalies, epilepsy, hypotonia, and neurobehavioral problems including autism
dc.type.none.fl_str_mv Text
Journal contribution
info:eu-repo/semantics/publishedVersion
text
contribution to journal
description <h3>Background</h3><p dir="ltr">PHF21A has been associated with intellectual disability and craniofacial anomalies based on its deletion in the Potocki-Shaffer syndrome region at 11p11.2 and its disruption in three patients with balanced translocations. In addition, three patients with de novo truncating mutations in PHF21A were reported recently. Here, we analyze genomic data from seven unrelated individuals with mutations in PHF21A and provide detailed clinical descriptions, further expanding the phenotype associated with PHF21A haploinsufficiency.</p><h3>Methods</h3><p dir="ltr">Diagnostic trio whole exome sequencing, Sanger sequencing, use of GeneMatcher, targeted gene panel sequencing, and MiSeq sequencing techniques were used to identify and confirm variants. RT-qPCR was used to measure the normal expression pattern of PHF21A in multiple human tissues including 13 different brain tissues. Protein-DNA modeling was performed to substantiate the pathogenicity of the missense mutation.</p><h3>Results</h3><p dir="ltr">We have identified seven heterozygous coding mutations, among which six are de novo (not maternal in one). Mutations include four frameshifts, one nonsense mutation in two patients, and one heterozygous missense mutation in the AT Hook domain, predicted to be deleterious and likely to cause loss of PHF21A function. We also found a new C-terminal domain composed of an intrinsically disordered region. This domain is truncated in six patients and thus likely to play an important role in the function of PHF21A, suggesting that haploinsufficiency is the likely underlying mechanism in the phenotype of seven patients. Our results extend the phenotypic spectrum of PHF21A mutations by adding autism spectrum disorder, epilepsy, hypotonia, and neurobehavioral problems. Furthermore, PHF21A is highly expressed in the human fetal brain, which is consistent with the neurodevelopmental phenotype.</p><h3>Conclusion</h3><p dir="ltr">Deleterious nonsense, frameshift, and missense mutations disrupting the AT Hook domain and/or an intrinsically disordered region in PHF21A were found to be associated with autism spectrum disorder, epilepsy, hypotonia, neurobehavioral problems, tapering fingers, clinodactyly, and syndactyly, in addition to intellectual disability and craniofacial anomalies. This suggests that PHF21A is involved in autism spectrum disorder and intellectual disability, and its haploinsufficiency causes a diverse neurological phenotype.</p><h2>Other Information</h2><p dir="ltr">Published in: Molecular Autism<br>License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1186/s13229-019-0286-0" target="_blank">https://dx.doi.org/10.1186/s13229-019-0286-0</a></p>
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identifier_str_mv 10.1186/s13229-019-0286-0
network_acronym_str Manara2
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oai_identifier_str oai:figshare.com:article/25904413
publishDate 2019
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spelling Disruption of PHF21A causes syndromic intellectual disability with craniofacial anomalies, epilepsy, hypotonia, and neurobehavioral problems including autismHyung-Goo Kim (728597)Jill A. Rosenfeld (9606199)Daryl A. Scott (10139232)Gerard Bénédicte (18615115)Jonathan D. Labonne (18615118)Jason Brown (253739)Marianne McGuire (4355386)Sonal Mahida (6413285)Sakkubai Naidu (804374)Jacqueline Gutierrez (7532777)Gaetan Lesca (6380633)Vincent des Portes (449415)Ange-Line Bruel (3178743)Arthur Sorlin (7532780)Fan Xia (219575)Yline Capri (3181152)Eric Muller (2212156)Dianalee McKnight (7532783)Erin Torti (7532786)Franz Rüschendorf (73756)Oliver Hummel (30411)Zeyaul Islam (5867387)Prasanna R. Kolatkar (124118)Lawrence C. Layman (13913559)Duchwan Ryu (7532795)Il-Keun Kong (85884)Suneeta Madan-Khetarpal (4355359)Cheol-Hee Kim (36752)Biological sciencesGeneticsPHF21ABHC80Intellectual disability (ID)Autism spectrum disorder (ASD)Neurodevelopmental disordersPotocki-Shaffer syndrome (PSS)AT Hook domainIntrinsically disordered region (IDR)KDM1A<h3>Background</h3><p dir="ltr">PHF21A has been associated with intellectual disability and craniofacial anomalies based on its deletion in the Potocki-Shaffer syndrome region at 11p11.2 and its disruption in three patients with balanced translocations. In addition, three patients with de novo truncating mutations in PHF21A were reported recently. Here, we analyze genomic data from seven unrelated individuals with mutations in PHF21A and provide detailed clinical descriptions, further expanding the phenotype associated with PHF21A haploinsufficiency.</p><h3>Methods</h3><p dir="ltr">Diagnostic trio whole exome sequencing, Sanger sequencing, use of GeneMatcher, targeted gene panel sequencing, and MiSeq sequencing techniques were used to identify and confirm variants. RT-qPCR was used to measure the normal expression pattern of PHF21A in multiple human tissues including 13 different brain tissues. Protein-DNA modeling was performed to substantiate the pathogenicity of the missense mutation.</p><h3>Results</h3><p dir="ltr">We have identified seven heterozygous coding mutations, among which six are de novo (not maternal in one). Mutations include four frameshifts, one nonsense mutation in two patients, and one heterozygous missense mutation in the AT Hook domain, predicted to be deleterious and likely to cause loss of PHF21A function. We also found a new C-terminal domain composed of an intrinsically disordered region. This domain is truncated in six patients and thus likely to play an important role in the function of PHF21A, suggesting that haploinsufficiency is the likely underlying mechanism in the phenotype of seven patients. Our results extend the phenotypic spectrum of PHF21A mutations by adding autism spectrum disorder, epilepsy, hypotonia, and neurobehavioral problems. Furthermore, PHF21A is highly expressed in the human fetal brain, which is consistent with the neurodevelopmental phenotype.</p><h3>Conclusion</h3><p dir="ltr">Deleterious nonsense, frameshift, and missense mutations disrupting the AT Hook domain and/or an intrinsically disordered region in PHF21A were found to be associated with autism spectrum disorder, epilepsy, hypotonia, neurobehavioral problems, tapering fingers, clinodactyly, and syndactyly, in addition to intellectual disability and craniofacial anomalies. This suggests that PHF21A is involved in autism spectrum disorder and intellectual disability, and its haploinsufficiency causes a diverse neurological phenotype.</p><h2>Other Information</h2><p dir="ltr">Published in: Molecular Autism<br>License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1186/s13229-019-0286-0" target="_blank">https://dx.doi.org/10.1186/s13229-019-0286-0</a></p>2019-10-22T03:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1186/s13229-019-0286-0https://figshare.com/articles/journal_contribution/Disruption_of_PHF21A_causes_syndromic_intellectual_disability_with_craniofacial_anomalies_epilepsy_hypotonia_and_neurobehavioral_problems_including_autism/25904413CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/259044132019-10-22T03:00:00Z
spellingShingle Disruption of PHF21A causes syndromic intellectual disability with craniofacial anomalies, epilepsy, hypotonia, and neurobehavioral problems including autism
Hyung-Goo Kim (728597)
Biological sciences
Genetics
PHF21A
BHC80
Intellectual disability (ID)
Autism spectrum disorder (ASD)
Neurodevelopmental disorders
Potocki-Shaffer syndrome (PSS)
AT Hook domain
Intrinsically disordered region (IDR)
KDM1A
status_str publishedVersion
title Disruption of PHF21A causes syndromic intellectual disability with craniofacial anomalies, epilepsy, hypotonia, and neurobehavioral problems including autism
title_full Disruption of PHF21A causes syndromic intellectual disability with craniofacial anomalies, epilepsy, hypotonia, and neurobehavioral problems including autism
title_fullStr Disruption of PHF21A causes syndromic intellectual disability with craniofacial anomalies, epilepsy, hypotonia, and neurobehavioral problems including autism
title_full_unstemmed Disruption of PHF21A causes syndromic intellectual disability with craniofacial anomalies, epilepsy, hypotonia, and neurobehavioral problems including autism
title_short Disruption of PHF21A causes syndromic intellectual disability with craniofacial anomalies, epilepsy, hypotonia, and neurobehavioral problems including autism
title_sort Disruption of PHF21A causes syndromic intellectual disability with craniofacial anomalies, epilepsy, hypotonia, and neurobehavioral problems including autism
topic Biological sciences
Genetics
PHF21A
BHC80
Intellectual disability (ID)
Autism spectrum disorder (ASD)
Neurodevelopmental disorders
Potocki-Shaffer syndrome (PSS)
AT Hook domain
Intrinsically disordered region (IDR)
KDM1A