Contribution of rare coding variants to microcephaly in individuals with neurodevelopmental disorders

Abstract Background Microcephaly, characterized by an abnormally small head size, frequently co-occurs with neurodevelopmental disorders (NDDs). While the genetic basis of NDDs has been widely investigated, the contribution of rare coding variants to microcephaly remains poorly understood. Methods W...

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Main Authors: Jihoon G. Yoon, Hyunsoo Jang, Seungbok Lee, Se Song Jang, Soojin Park, Jaeso Cho, Minji Kim, Jiye Han, Hyounji Yun, Man Jin Kim, Soo Yeon Kim, Woo Joong Kim, Anna Cho, Jin Sook Lee, Murim Choi, Alberto Fernandez-Jaen, Sebastian Silva, Reinaldo Uribe-San-Martín, Christian Cantillano, Noriko Miyake, Byung Chan Lim, Jung Min Ko, Ki Joong Kim, Ki-Jun Yoon, Jong-Hee Chae
Format: Article
Language:English
Published: BMC 2025-08-01
Series:Genome Medicine
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Online Access:https://doi.org/10.1186/s13073-025-01513-w
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author Jihoon G. Yoon
Hyunsoo Jang
Seungbok Lee
Se Song Jang
Soojin Park
Jaeso Cho
Minji Kim
Jiye Han
Hyounji Yun
Man Jin Kim
Soo Yeon Kim
Woo Joong Kim
Anna Cho
Jin Sook Lee
Murim Choi
Alberto Fernandez-Jaen
Sebastian Silva
Reinaldo Uribe-San-Martín
Christian Cantillano
Noriko Miyake
Byung Chan Lim
Jung Min Ko
Ki Joong Kim
Ki-Jun Yoon
Jong-Hee Chae
author_facet Jihoon G. Yoon
Hyunsoo Jang
Seungbok Lee
Se Song Jang
Soojin Park
Jaeso Cho
Minji Kim
Jiye Han
Hyounji Yun
Man Jin Kim
Soo Yeon Kim
Woo Joong Kim
Anna Cho
Jin Sook Lee
Murim Choi
Alberto Fernandez-Jaen
Sebastian Silva
Reinaldo Uribe-San-Martín
Christian Cantillano
Noriko Miyake
Byung Chan Lim
Jung Min Ko
Ki Joong Kim
Ki-Jun Yoon
Jong-Hee Chae
author_sort Jihoon G. Yoon
collection DOAJ
description Abstract Background Microcephaly, characterized by an abnormally small head size, frequently co-occurs with neurodevelopmental disorders (NDDs). While the genetic basis of NDDs has been widely investigated, the contribution of rare coding variants to microcephaly remains poorly understood. Methods We investigated the relationships between head circumference and rare coding variants in 418 individuals with microcephaly, analyzing data from 1050 exomes (312 trios and 106 proband-only samples). Participants were classified into primary microcephaly (PM) and secondary microcephaly (SM) groups, and their clinical and genetic characteristics were systematically assessed. The functional impact of high-priority candidate genes, RTF1 and ASAP2, was further validated using neural progenitor cells (NPCs) and human forebrain organoid models. Results Exome sequencing revealed 142 causative and 12 candidate genes associated with microcephaly. Pathway analyses indicated that PM genes are linked to early phases of brain development, whereas SM genes are more associated with later stages of neuronal maturation. In addition, the PM group had a significantly higher proportion of autosomal recessive disorders and exhibited more severe microcephaly than the SM group. Notably, females displayed greater microcephaly severity than males, primarily attributable to differences in the origin of the allele and inheritance patterns on the X chromosome. Functional experiments using CRISPR-Cas9 knockout in NPCs and brain organoids demonstrated reduced NPC proliferation, supporting the essential role of RTF1 and ASAP2 in brain development. Conclusions This study sheds light on the complex genetic architecture of microcephaly, emphasizing the impact of rare coding variants on brain development and delineating distinct clinical and molecular profiles underlying PM and SM.
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spelling doaj-art-9d7e3352c69d44ef9562c7280a99660f2025-08-20T04:02:56ZengBMCGenome Medicine1756-994X2025-08-0117112010.1186/s13073-025-01513-wContribution of rare coding variants to microcephaly in individuals with neurodevelopmental disordersJihoon G. Yoon0Hyunsoo Jang1Seungbok Lee2Se Song Jang3Soojin Park4Jaeso Cho5Minji Kim6Jiye Han7Hyounji Yun8Man Jin Kim9Soo Yeon Kim10Woo Joong Kim11Anna Cho12Jin Sook Lee13Murim Choi14Alberto Fernandez-Jaen15Sebastian Silva16Reinaldo Uribe-San-Martín17Christian Cantillano18Noriko Miyake19Byung Chan Lim20Jung Min Ko21Ki Joong Kim22Ki-Jun Yoon23Jong-Hee Chae24Department of Genomic Medicine, Rare Disease Center, Seoul National University Children’s Hospital and Seoul National University College of MedicineDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)Department of Genomic Medicine, Rare Disease Center, Seoul National University Children’s Hospital and Seoul National University College of MedicineDepartment of Pediatrics, Seoul National University Children’s HospitalDepartment of Pediatrics, Seoul National University Children’s HospitalDepartment of Genomic Medicine, Rare Disease Center, Seoul National University Children’s Hospital and Seoul National University College of MedicineDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)Department of Genomic Medicine, Rare Disease Center, Seoul National University Children’s Hospital and Seoul National University College of MedicineDepartment of Genomic Medicine, Rare Disease Center, Seoul National University Children’s Hospital and Seoul National University College of MedicineDepartment of Pediatrics, Seoul National University Children’s HospitalDepartment of Pediatrics, Seoul National University Bundang HospitalDepartment of Pediatrics, Seoul National University Hospital Child Cancer and Rare Disease Administration, Seoul National University Children’s HospitalDepartment of Biomedical Sciences, Seoul National University College of MedicineDepartment of Pediatric Neurology, Neurogenetic Section, Hospital Universitario Quironsalud, Universidad EuropeaChild Neurology Service, Hospital de Puerto MonttDepartamento de Neurología, Pontificia Universidad Católica de ChileNational Reference Center for Epilepsy, Hospital Dr. Sótero del RíoDepartment of Human Genetics, National Institute of Global Health and Medicine, Japan Institute for Health SecurityDepartment of Pediatrics, Seoul National University Children’s HospitalDepartment of Pediatrics, Seoul National University Children’s HospitalDepartment of Pediatrics, Seoul National University Children’s HospitalDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)Department of Genomic Medicine, Rare Disease Center, Seoul National University Children’s Hospital and Seoul National University College of MedicineAbstract Background Microcephaly, characterized by an abnormally small head size, frequently co-occurs with neurodevelopmental disorders (NDDs). While the genetic basis of NDDs has been widely investigated, the contribution of rare coding variants to microcephaly remains poorly understood. Methods We investigated the relationships between head circumference and rare coding variants in 418 individuals with microcephaly, analyzing data from 1050 exomes (312 trios and 106 proband-only samples). Participants were classified into primary microcephaly (PM) and secondary microcephaly (SM) groups, and their clinical and genetic characteristics were systematically assessed. The functional impact of high-priority candidate genes, RTF1 and ASAP2, was further validated using neural progenitor cells (NPCs) and human forebrain organoid models. Results Exome sequencing revealed 142 causative and 12 candidate genes associated with microcephaly. Pathway analyses indicated that PM genes are linked to early phases of brain development, whereas SM genes are more associated with later stages of neuronal maturation. In addition, the PM group had a significantly higher proportion of autosomal recessive disorders and exhibited more severe microcephaly than the SM group. Notably, females displayed greater microcephaly severity than males, primarily attributable to differences in the origin of the allele and inheritance patterns on the X chromosome. Functional experiments using CRISPR-Cas9 knockout in NPCs and brain organoids demonstrated reduced NPC proliferation, supporting the essential role of RTF1 and ASAP2 in brain development. Conclusions This study sheds light on the complex genetic architecture of microcephaly, emphasizing the impact of rare coding variants on brain development and delineating distinct clinical and molecular profiles underlying PM and SM.https://doi.org/10.1186/s13073-025-01513-wMicrocephalyHead circumferenceNeurodevelopmental disorderExome sequencingBrain organoids
spellingShingle Jihoon G. Yoon
Hyunsoo Jang
Seungbok Lee
Se Song Jang
Soojin Park
Jaeso Cho
Minji Kim
Jiye Han
Hyounji Yun
Man Jin Kim
Soo Yeon Kim
Woo Joong Kim
Anna Cho
Jin Sook Lee
Murim Choi
Alberto Fernandez-Jaen
Sebastian Silva
Reinaldo Uribe-San-Martín
Christian Cantillano
Noriko Miyake
Byung Chan Lim
Jung Min Ko
Ki Joong Kim
Ki-Jun Yoon
Jong-Hee Chae
Contribution of rare coding variants to microcephaly in individuals with neurodevelopmental disorders
Genome Medicine
Microcephaly
Head circumference
Neurodevelopmental disorder
Exome sequencing
Brain organoids
title Contribution of rare coding variants to microcephaly in individuals with neurodevelopmental disorders
title_full Contribution of rare coding variants to microcephaly in individuals with neurodevelopmental disorders
title_fullStr Contribution of rare coding variants to microcephaly in individuals with neurodevelopmental disorders
title_full_unstemmed Contribution of rare coding variants to microcephaly in individuals with neurodevelopmental disorders
title_short Contribution of rare coding variants to microcephaly in individuals with neurodevelopmental disorders
title_sort contribution of rare coding variants to microcephaly in individuals with neurodevelopmental disorders
topic Microcephaly
Head circumference
Neurodevelopmental disorder
Exome sequencing
Brain organoids
url https://doi.org/10.1186/s13073-025-01513-w
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