Case Report Open Access
Copyright ©The Author(s) 2022. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Clin Cases. Jan 14, 2022; 10(2): 607-617
Published online Jan 14, 2022. doi: 10.12998/wjcc.v10.i2.607
Novel compound heterozygous GPR56 gene mutation in a twin with lissencephaly: A case report
Wen-Xin Lin, Ying-Ying Chai, Ting-Ting Huang, Xia Zhang, Guo Zheng, Gang Zhang, Fang Peng, Yan-Jun Huang
Wen-Xin Lin, Ying-Ying Chai, Ting-Ting Huang, Xia Zhang, Guo Zheng, Gang Zhang, Yan-Jun Huang, Department of Neurology, Children’s Hospital of Nanjing Medical University, Nanjing 210000, Jiangsu Province, China
Fang Peng, Department of Neurology, Huashan Hospital, Fudan University, Shanghai 200040, China
ORCID number: Wen-Xin Lin (0000-0003-0591-3880); Ying-Ying Chai (0000-0002-5270-4419); Ting-Ting Huang (0000-0001-5177-416X); Xia Zhang (0000-0002-1248-6330); Guo Zheng (0000-0001-7525-9680); Gang Zhang (0000-0001-5729-7667); Fang Peng (0000-0003-4992-8937); Yanjun Huang (0000-0001-5270-0867).
Author contributions: Lin WX performed the data analysis and drafted the manuscript; Chai YY conducted the molecular genetic studies and drafted the manuscript; Huang TT, Zhang X, Zheng G, Zhang G and Peng F participated in the design of the study; Huang YJ conceived the study, participated in its design and coordination and helped to draft the manuscript; all authors read and approved the final manuscript.
Supported by the Six Talent Peaks Project in Jiangsu Province, No. 2016-YY-055.
Informed consent statement: Written informed consent for publication was obtained from the parents.
Conflict-of-interest statement: The authors report having no conflicts of interest in relation to this article.
CARE Checklist (2016) statement: The authors have read the CARE Checklist (2016), and the manuscript was prepared and revised according to the CARE Checklist (2016).
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Yan-Jun Huang, PhD, Additional Professor, Chief Physician, Department of Neurology, Children’s Hospital of Nanjing Medical University, No. 72 Guangzhou Road, Nanjing 210000, Jiangsu Province, China. njhuang2013@126.com
Received: January 31, 2021
Peer-review started: January 31, 2021
First decision: July 16, 2021
Revised: July 19, 2021
Accepted: December 9, 2021
Article in press: December 9, 2021
Published online: January 14, 2022

Abstract
BACKGROUND

Lissencephaly (LIS) is a malformation of cortical development with broad gyri, shallow sulci and thickened cortex characterized by developmental delays and seizures. Currently, 20 genes have been implicated in LIS. However, GRP56-related LIS has never been reported. GRP56 is considered one of the causative genes for bilateral frontoparietal polymicrogyria. Here, we report a twin infant with LIS and review the relevant literature. The twins both carried the novel compound heterozygous GPR56 mutations.

CASE SUMMARY

A 5-mo-old female infant was hospitalized due to repeated convulsions for 1 d. The patient had a flat head deformity that manifested as developmental delays and a sudden onset of generalized tonic-clonic seizures at 5 mo without any causes. The electroencephalography was normal. Brain magnetic resonance imaging revealed a simple brain structure with widened and thickened gyri and shallow sulci. The white matter of the brain was significantly reduced. Patchy long T1 and T2 signals could be seen around the ventricles, which were expanded, and the extracerebral space was widened. Genetic testing confirmed that the patient carried the GPR56 gene compound heterozygous mutations c.228delC (p.F76fs) and c.1820_1821delAT (p.H607fs). The unaffected father carried a heterozygous c.1820_1821delAT mutation, and the unaffected mother carried a heterozygous c.228delC mutation. The twin sister carried the same mutations as the proband. The patient was diagnosed with LIS.

CONCLUSION

This is the first case report of LIS that is likely caused by mutations of the GPR56 gene.

Key Words: Lissencephaly, Epilepsy, GPR56 mutations, Compound heterozygous mutations, Case report

Core Tip: We report a twin infant with lissencephaly (LIS). The twins both carried the novel compound heterozygous GPR56 mutations, p.F76fs and p.H607fs, which have not been reported in the Human Gene Mutation Database. To our knowledge, this is the first case of GRP56-related LIS. Therefore, GPR56 gene mutations may lead to LIS.



INTRODUCTION

Lissencephaly (LIS) is a group of abnormal cerebral cortical dysplasias caused by the defective migration of neurons. It can be diagnosed clinically by neuroimaging. It is characterized by thickening of the cerebral cortex, widening of the gyri, and disappearance or shallowness of the sulci. The complete disappearance of the sulci and gyri showing smooth surface of the brain is called agyria and is seen in severe cases[1]. According to the neuroimaging, LIS is divided into six grades, ranging from severe agyria (grade 1) to mild subcortical band heterotopias (grade 6). The severity of nerve damage is closely related to the grade of LIS and cortical thickening, and the mortality rate of severe LIS is high[2]. In the early stages, patients often exhibit developmental delays and hypotonia, followed by seizures, and a severe intellectual disability eventually. Although a LIS patient may develop normally in the neonatal period, many neonates suffer from persistent feeding problems and different types of epilepsy, which are difficult to cure[3]. An individual with mild LIS and normal intelligence has been reported[4]. Currently, 20 genes have been implicated in LIS. Many of these genes are microtubule genes[5,6].

GPR56 (OMIM#606854, NM_0001145773) encodes an orphan G protein-coupled receptor (GPCR) that is extensively expressed in the nervous system and is essential for the normal development of the cerebral cortex and cerebellar morphology[7-9]. The reported mutations of the GPR56 gene have been confirmed to be related to bilateral frontoparietal polymicrogyria (BFPP)[10].

Herein, we report a twin infant with LIS who came from a nonconsanguineous family. The twins both carried a novel compound heterozygous GPR56 mutation. To our knowledge, this is the first case of GRP56-related LIS.

CASE PRESENTATION
Chief complaints

A 5-mo-old female infant was hospitalized due to repeated convulsions for 1 d.

History of present illness

The patient was admitted to the Children’s Hospital of Nanjing Medical University due to repeated convulsions. The patient had a sudden onset of generalized tonic-clonic seizures without any causes. In addition, she had a flat head deformity and developmental delays.

History of past illness

The patient had no history of past illness.

Personal and family history

The patient was the first child of nonconsanguineous Chinese parents. She was delivered by cesarean section due to twin pregnancy at 32 wk of gestation, with a birth weight of 2.6 kg. No intrauterine distress or postnatal asphyxia had occurred. She had a twin sister with LIS.

Physical examination

The patient showed a flat head deformity. The neurological examination was normal. There were no other abnormal signs.

Laboratory examinations

The electroencephalography and laboratory findings (full blood count, liver, kidney and thyroid function tests, creatine kinase, uric acid, metabolic study and chromosome karyotyping) were normal.

Imaging examinations

Brain magnetic resonance imaging (MRI) revealed a simple brain structure, with widened and thickened gyri and shallow sulci. The white matter of the brain was significantly reduced. The patchy long T1 and long T2 signals could be seen around the ventricles, which were expanded, and the extracerebral space was widened (Figure 1).

Figure 1
Figure 1 Brain magnetic resonance imaging of the proband revealed a simple brain structure, with widened and thickened gyri and shallow sulci.
FINAL DIAGNOSIS

According to the clinical characteristics, imaging and genetic test findings (Figure 2), the infant was diagnosed with LIS.

Figure 2
Figure 2 Sanger sequencing of the proband and her family members.
TREATMENT

During the hospital stay, the patient had no epileptic seizures. She received rehabilitation, but anti-epileptic treatment was refused.

OUTCOME AND FOLLOW-UP

The patient experienced repeated convulsions after she was discharged from hospital. The convulsions occurred once a day to more than ten times a day without any causes, each episode lasting several minutes. She died 3 mo later.

DISCUSSION

The GPR56 gene spans 45 kb and consists of 14 exons encoding an orphan GPCR of 693 amino acids[7,11]. GPR56 is a member of the adhesion GPCR family, which has an N- and a C-terminal fragment and a GPCR proteolytic site[12]. In the central nervous system, GPR56 plays an important role in the normal development of the cerebral cortex and cerebellar morphogenesis[8]. In the peripheral nervous system, GPR56 can regulate the formation and maintenance of myelin sheaths[13]. Therefore, the normal expression of GPR56 is essential for the function of the nervous system.

It is known that mutations of the GPR56 gene are related to BFPP (Table 1). The clinical manifestations of BFPP are overall growth retardation and seizures. MRI shows symmetrical polygyria (the frontal parietal area is the most serious part), ventricular enlargement, and bilateral white matter changes. Twenty-eight pathogenic GPR56 mutations related to the BFPP phenotype have been reported[11,14]. The affected individuals inherit the mutants in an autosomal recessive mode. The majority of missense mutations resulted in similar clinical symptoms, indicating that the similar phenotype might be caused by the same mechanism. However, the mechanism remains unclear, although it may involve GPR56 trafficking and a decrease in receptor levels at the cell membrane[15-17]. GPR56 knockdown did not affect the migration of neural progenitor cells, while GPR56 overexpression inhibited the migration of neural progenitor cells. This mechanism might occur through the reorganization of cerebral cortex actin to change the cell morphology and regulate neural progenitor cell behavior[8]. LIS is caused by premature stop of neuronal migration, which might explain the mechanism of the GPR56 mutations causing LIS in the present case.

Table 1 Summary of GPR56 mutations.
Ref.
Mutation
Exon/intron
Case number
Ethnicity
Consanguinity
Motor delay
Cognitive delay
Seizure
MRI
Gyri
White matter abnormalities    
Brainstem/cerebellum
Piao et al[10,11], 2004 and 2005c.112C>T (p.R38W)Exon 32Arabic (Qatar)First cousin+ModerateGTC, myoclonicBFPPPatchy signal changeSmall brainstem
+NA+
1Arabic (UAE)First cousin++NABFPPReduced volume, patchy signal changeSlightly small pons and vermis
c.113G>A (p.R38Q)Exon 31TurkishFirst cousin+++BFPPSeverely reduced volume, patchy signal changeSmall pons and vermis
c.263A>G (p.Y88C)Exon 32French CanadianN++NABFPPReduced volume, patchy signal changeSmall pons, small/dysplastic cerebellum
c.739-746 delCAGGACC (p.Q246Tfx*72)Exon 52IndianN++Blank episodesBFPPReduced volume, patchy signal changeSlightly small pons and vermis
++AS
1PakistaniFirst cousinSevereSevereGeneralizedBFPPPatchy radiolucency Small cerebellum
1AfghaniFirst cousinModerate+NABFPPReduced volume, patchy signal changeSmall pons and superior vermis
c.E5- 1G>C (NA)Exon 52PalestinianN++Episodes of startlesBFPPReduced volume, periventricular signal changeSmall pons and superior vermis
c.1036T>A(p.C346S)Exon 82PalestinianFirst cousin++NABFPPReduced volume, patchy signal changeSmall pons and cerebellum
1PalestinianFirst cousin+Severe+BFPPReduced volume, frontal subcortical signal changeSmall brainstem and cerebellum
c.1046G>C(p.W349S)Exon 82Israeli JewishFirst cousin++GTCBFPPReduced volume, patchy signal changeSmall pons and vermis
++MyoclonicBFPP
1Israeli JewishN+Severe+BFPPPatchy signal change Small vermis
c.IVS9+3G>C (NA)Intron 93PalestinianFirst cousin++FS, atonic-dropBFPPPatchy signal changeSlightly small pons and superior vermis
+ModerateGTC, ASBFPP
SevereSevereFS, GTCBFPP
2PalestinianFirst cousin+SevereGTC, atonicBFPPPatchy signal changeSmall pons and superior vermis
+SevereNoBFPP
c.1693C>T (p.R565W)Exon 133Arabic (Bedouin)C+SevereGTC, myoclonicBFPPReduced volume, patchy signal changeSmall vermis
1ItalianSecond cousin+++BFPPReduced volume, patchy signal changeSlightly small vermis
c.1919T>G (p.L640R)Exon 131HispanicN+++BFPPMildly reduced volume, patchy signal changeSlightly small cerebellar hemispheres
Parrini et al[18], 2009c.97C>G (p.R33P)Exon 22TurkishC+SevereAtypical absences, GTC, tonicBFPPNANA
+SevereTonic, atypical absences, recurrent nonconvulsive status epilepticusBFPPPatchy signal changeNA
c.235C>T (R79X)Exon 21ItalianC+SevereInfantile spasms, tonic and atonic seizuresBFPPPatchy signal changeNA
c.1693C>T (p.R565W)Exon 131ItalianC+SevereTonic atonic GTC, atypical absences, recurrent nonconvulsive statusepilepticusBFPPPatchy signal changeSlightly small vermis
Bahi-Buisson et al[19], 2010c.174-175insC (p.E59Rfs*24)Exon 32NACNASevere+NANANA
Walking at 4 yrSevereFocal seizuresBFPPPatchy periventricular predominanceHypoplastic pons
c.272G>A (p.C91Y)Exon 32NACWalking at 2 yrSevereNABFPPPatchy Hypoplastic pons
Walking at 2 yrSevereGTC/atypical absence, atonic seizuresBFPPPatchy periventricular and frontal predominanceHypoplastic pons, Cyst in the ventral pons
c.367C>T (p.Q123X)Exon 31NAC+SevereFocal seizures, GTCBFPPPatchy periventricular and frontal predominanceHypoplastic pons, Cyst in the ventral pons
c.671delA (p.D224Wfs*96)Exon 53NACWalking at 4 yrSevereGTCBFPPPatchy periventricular and frontal predominanceHypoplastic pons
Walking at 18 moSevereGTCBFPP
Sitting without supportSevereGTCBFPPDiffuseHypoplastic pons
c.1215-1216delC (p.L406S406fs*41)Exon 101NACWalking acquired but subsequently lost (11 yr)Severe+BFPPPatchyHypoplastic pons
c.1254C>G (p.C418W)Exon 103PakistaniFirst cousinWalking at 5 yrSevereGTCBFPPDiffuseHypoplastic pons
Walking at 5 yrSevereGTCBFPPPatchy with subcortical and frontal predominance, reduced volumeSeverely hypoplastic pons with posterior concavity, cyst in the ventral pons
NANANANANANA
c.1345delCTG (p.L449del)Exon 111NACWalking at 3 yrSevereAtypical absenceBFPPPatchy with subcortical predominanceSeverely hypoplastic pons with posterior concavity
c.1453C>T (p.S485P)Exon 112NACWalking at 18 moSevereFocal seizures, generalized tonic seizuresBFPPPatchy with subcortical and frontal predominanceHypoplastic pons
Walking at 18 moSevereFocal seizuresBFPP
Luo et al[20], 2011c.1486G>A (p.E496K)NA1YemeniFirst cousinWalkingSevereTonic-clonic seizuresBFPPAsymmetric areas of abnormal signal in the white matter of both cerebral hemispheresMild hypoplasia of the inferior cerebellar vermis and pons
Quattrocchi et al[16], 2013c.105C>A (p.C35X)Exon 21NANAAtaxic gaitSevereFocal seizures, myoclonic BFPPPatchy subcortical and periventricular white matter abnormalitiesMildly hypoplastic cerebellar vermis, flattening of the ventral aspect of the pons, hemispheric cerebellar cysts, vermian cysts
c.429G>A (p.W143X)Exon 21NANAAtaxic gaitModerateNoBFPPPatchy subcortical and periventricular white matter abnormalitiesMildly hypoplastic cerebellar vermis, flattening of the ventral aspect of the pons, hemispheric cerebellar cysts, vermian cysts
c.1453C>T (p.S485P)Exon 112NANAWalking at 18 moSevereGTS, focal seizuresBFPPPatchy subcortical and periventricular white matter abnormalitiesHypoplastic pons and superior vermis, hemispheric cerebellar cysts, vermian cysts
Walking at 22 moSevereFocal seizuresBFPPPatchy subcortical and periventricular white matter abnormalitiesHypoplastic pons and superior vermis, hemispheric cerebellar cysts, vermian cysts
c.1796-1801delTGCGCC/insAGATCCTGTGGGCAGAT (premature stop codon at position 614)Exon 121NANAAtaxic gaitModerateNoBFPPPatchy subcortical and periventricular white matter abnormalitiesFlattening of the ventral aspect of the pons, hemispheric cerebellar cysts
Fujii et al[21], 2014c.107G>A and c.113G>A(p.S36N and p.R38Q)Exon 21JapaneseNAble to walk with helpSevereComplex partial seizures, tonic seizures, epileptic spasmsBFPPPatchy high signals in the frontal subcortical Hypoplastic pons
Desai et al[22], 2015c.113G>A (p.R38Q)Exon 31Indian (Marathi)CMode-rateModerateComplex febrile seizuresBFPPDiffuseMild thinning and cerebellar cysts
c.739–746 delCAGGACC (p.Q246Tfx*72)Exon 41Indian (Punjabi)NSevereMildNoBFPPFrontal and periventricularMild thinning and cerebellar cysts
c.739–746 delCAGGACC (p.Q246Tfx*72)Exon 41Indian (Sindhi)NSevereModerateNoBFPPFrontal and periventricularInferior vermian hypoplasia; cerebellar cyst
c.1426 C>T (p.R476X)Exon 121Indian (Gujarati)CSevereSevereGeneralized seizuresBFPPDiffuseMild thinning and cerebellar cysts
Santos-Silva et al[17], 2015811C > T (R271X)Exon 61CaucasianNSevereSevereHot water epilepsyBFPPReduced volume, patchy signal changeHypoplasia of the pons and cerebellar vermis
Öncü-Öner et al[14], 2018811C > T (R271X)Exon 61NACSevereSevereFocal onset bilateral tonic-clonic seizureBFPPYesThin brainstem and normal cerebellar structure
Current reportc.228delC and c.1820-1821del AT (p.F76fs and p.H607fs)Exon 6 and Exon 132ChineseN+SevereGTCLISReduced volume, patchy signal changeNormal
++NoLISNANA

The development of the brain is a delicate and complex physiological process, and the proper migration of neurons is one of the most critical steps. LIS is brain dysplasia caused by the premature stop of neuronal migration. Type I LIS is characterized by a thickened cerebral cortex (10-20 mm, whereas normal is 4 mm), but no other brain development malformations, such as severe congenital microcephaly, corpus callosum hypoplasia, or cerebellar hypoplasia[2]. Microscopically, the cerebral cortex in LIS is divided into four thick and dysplastic layers: The molecular layer, the superficial cellular layer, the cell spare layer, and the deeper cellular layer; the normal cerebral cortex has six layers[1].

Currently, 20 genes have been reported to be associated with LIS, and many of them are microtubule genes[5,6]. In a cohort study of 811 patients with LIS, the overall mutation frequency of the entire cohort was 81%, of which LIS1 accounted for 40%, followed by DCX (23%), TUBA1A (5%), and DYNC1H1 (3%). Other genes accounted for 1% or less. Interestingly, the cause of LIS in 19% of the patients was unknown, which indicates that additional genes are involved and need to be discovered[6]. There have been no other reports of LIS caused by GPR56 gene mutations. Therefore, the relationship between LIS and GPR56 still needs further research.

There is no specific treatment method for LIS. Current treatments typically involve symptomatic relief, such as anti-epileptic treatment and rehabilitation training. Studies in animal models have shown that it might be possible to restart neuronal migration by re-expressing the missing/nonfunctional genes after birth[2]. Even if the degree of cortical deformity is partially improved, it may significantly decrease seizure frequency and clinical severity[2]. Therefore, with the advances in genetic testing and medical technology, the diagnosis and treatment of LIS will continue to be improved and optimized.

CONCLUSION

The compound mutations in the GPR56 gene identified in the twin sisters with LIS were novel and unreported mutations. This finding has broadened our knowledge of the clinical manifestations of LIS and increased our understanding of GPR56. Genetic testing is necessary when patients suffer from LIS symptoms.

ACKNOWLEDGEMENTS

We sincerely appreciate the patients and their parents for their help and willingness in this study.

Footnotes

Provenance and peer review: Unsolicited article; Externally peer reviewed.

Peer-review model: Single blind

Specialty type: Pediatrics

Country/Territory of origin: China

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P-Reviewer: Idiculla PS S-Editor: Zhang H L-Editor: A P-Editor: Zhang H

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