Consensus interpretation of the p.Met34Thr and p.Val37Ile variants in GJB2 by the ClinGen Hearing Loss Expert Panel.


Journal

Genetics in medicine : official journal of the American College of Medical Genetics
ISSN: 1530-0366
Titre abrégé: Genet Med
Pays: United States
ID NLM: 9815831

Informations de publication

Date de publication:
11 2019
Historique:
received: 09 12 2018
accepted: 24 04 2019
pubmed: 5 6 2019
medline: 28 4 2020
entrez: 5 6 2019
Statut: ppublish

Résumé

Pathogenic variants in GJB2 are the most common cause of autosomal recessive sensorineural hearing loss. The classification of c.101T>C/p.Met34Thr and c.109G>A/p.Val37Ile in GJB2 are controversial. Therefore, an expert consensus is required for the interpretation of these two variants. The ClinGen Hearing Loss Expert Panel collected published data and shared unpublished information from contributing laboratories and clinics regarding the two variants. Functional, computational, allelic, and segregation data were also obtained. Case-control statistical analyses were performed. The panel reviewed the synthesized information, and classified the p.Met34Thr and p.Val37Ile variants utilizing professional variant interpretation guidelines and professional judgment. We found that p.Met34Thr and p.Val37Ile are significantly overrepresented in hearing loss patients, compared with population controls. Individuals homozygous or compound heterozygous for p.Met34Thr or p.Val37Ile typically manifest mild to moderate hearing loss. Several other types of evidence also support pathogenic roles for these two variants. Resolving controversies in variant classification requires coordinated effort among a panel of international multi-institutional experts to share data, standardize classification guidelines, review evidence, and reach a consensus. We concluded that p.Met34Thr and p.Val37Ile variants in GJB2 are pathogenic for autosomal recessive nonsyndromic hearing loss with variable expressivity and incomplete penetrance.

Identifiants

pubmed: 31160754
doi: 10.1038/s41436-019-0535-9
pii: S1098-3600(21)01066-2
pmc: PMC7235630
mid: NIHMS1586971
doi:

Substances chimiques

Connexins 0
GJB2 protein, human 0
Connexin 26 127120-53-0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2442-2452

Subventions

Organisme : NIDCD NIH HHS
ID : R01 DC011835
Pays : United States
Organisme : NIDCD NIH HHS
ID : R03 DC013866
Pays : United States
Organisme : NIMHD NIH HHS
ID : L60 MD003721
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC015052
Pays : United States
Organisme : NHGRI NIH HHS
ID : U41 HG006834
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR059049
Pays : United States
Organisme : NIAMS NIH HHS
ID : T32 AR069512
Pays : United States
Organisme : NHGRI NIH HHS
ID : U01 HG008666
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01DC011835
Pays : United States
Organisme : NIDCD NIH HHS
ID : R03DC013866
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01DC015052
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007748
Pays : United States

Investigateurs

Hela Azaiez (H)
Kevin T Booth (KT)
Richard J Smith (RJ)
Anne B Giersch (AB)
Cynthia C Morton (CC)
Xue Z Liu (XZ)
Mustafa Tekin (M)
Yu Lu (Y)
Huijun Yuan (H)
Hideki Mutai (H)
Lisa Schimmenti (L)

Références

Wang NK, Chiang JPW. Increasing evidence of combinatory variant effects calls for revised classification of low-penetrance alleles. Genet Med. 2018 Nov 2; https://doi.org/10.1038/s41436-018-0347-3 [Epub ahead of print].
Richards S, Aziz N, Bale S, et al. Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genet Med. 2015;17:405–424.
doi: 10.1038/gim.2015.30
Oza AM, DiStefano MT, Hemphill SE, et al. Expert specification of the ACMG/AMP variant interpretation guidelines for genetic hearing loss. Hum Mutat. 2018;39:1593–1613.
doi: 10.1002/humu.23630
Kelsell DP, Dunlop J, Stevens HP, et al. Connexin 26 mutations in hereditary non-syndromic sensorineural deafness. Nature. 1997;387:80–83.
doi: 10.1038/387080a0
Scott DA, Kraft ML, Carmi R, et al. Identification of mutations in the connexin 26 gene that cause autosomal recessive nonsyndromic hearing loss. Hum Mutat. 1998;11:387–394.
doi: 10.1002/(SICI)1098-1004(1998)11:5<387::AID-HUMU6>3.0.CO;2-8
Scott DA, Kraft ML, Stone EM, et al. Connexin mutations and hearing loss. Nature. 1998;391:32.
doi: 10.1038/34079
Wilcox SA, Saunders K, Osborn AH, et al. High frequency hearing loss correlated with mutations in the GJB2 gene. Hum Genet. 2000;106:399–405.
doi: 10.1007/s004390000273
Houseman MJ, Ellis LA, Pagnamenta A, et al. Genetic analysis of the connexin-26 M34T variant: identification of genotype M34T/M34T segregating with mild-moderate non-syndromic sensorineural hearing loss. J Med Genet. 2001;38:20–25.
doi: 10.1136/jmg.38.1.20
Cucci RA, Prasad S, Kelley PM, et al. The M34T allele variant of connexin 26. Genet Test. 2000;4:335–344.
doi: 10.1089/109065700750065063
Kelley PM, Harris DJ, Comer BC, et al. Novel mutations in the connexin 26 gene (GJB2) that cause autosomal recessive (DFNB1) hearing loss. Am J Hum Genet. 1998;62:792–799.
doi: 10.1086/301807
Abe S, Usami S, Shinkawa H, et al. Prevalent connexin 26 gene (GJB2) mutations in Japanese. J Med Genet. 2000;37:41–43.
doi: 10.1136/jmg.37.1.41
Griffith AJ, Chowdhry AA, Kurima K, et al. Autosomal recessive nonsyndromic neurosensory deafness at DFNB1 not associated with the compound-heterozygous GJB2 (connexin 26) genotype M34T/167delT. Am J Hum Genet. 2000;67:745–749.
doi: 10.1086/303045
Feldmann D, Denoyelle F, Loundon N, et al. Clinical evidence of the nonpathogenic nature of the M34T variant in the connexin 26 gene. Eur J Hum Genet. 2004;12:279–284.
doi: 10.1038/sj.ejhg.5201147
Pollak A, Skorka A, Mueller-Malesinska M, et al. M34T and V37I mutations in GJB2 associated hearing impairment: evidence for pathogenicity and reduced penetrance. Am J Med Genet A. 2007;143A:2534–2543.
doi: 10.1002/ajmg.a.31982
Wu CC, Tsai CH, Hung CC, et al. Newborn genetic screening for hearing impairment: a population-based longitudinal study. Genet Med. 2017;19:6–12.
doi: 10.1038/gim.2016.66
Chai Y, Chen D, Sun L, et al. The homozygous p.V37I variant of GJB2 is associated with diverse hearing phenotypes. Clin Genet. 2015;87:350–355.
doi: 10.1111/cge.12387
White TW, Deans MR, Kelsell DP, Paul DL. Connexin mutations in deafness. Nature. 1998;394:630–631.
doi: 10.1038/29202
Skerrett IM, Di WL, Kasperek EM, et al. Aberrant gating, but a normal expression pattern, underlies the recessive phenotype of the deafness mutant Connexin26M34T. FASEB J. 2004;18:860–862.
doi: 10.1096/fj.03-0763fje
Palmada M, Schmalisch K, Bohmer C, et al. Loss of function mutations of the GJB2 gene detected in patients with DFNB1-associated hearing impairment. Neurobiol Dis. 2006;22:112–118.
doi: 10.1016/j.nbd.2005.10.005
Martin PE, Coleman SL, Casalotti SO, et al. Properties of connexin26 gap junctional proteins derived from mutations associated with non-syndromal heriditary deafness. Hum Mol Genet. 1999;8:2369–2376.
doi: 10.1093/hmg/8.13.2369
Thonnissen E, Rabionet R, Arbones ML, et al. Human connexin26 (GJB2) deafness mutations affect the function of gap junction channels at different levels of protein expression. Hum Genet. 2002;111:190–197.
doi: 10.1007/s00439-002-0750-2
Bicego M, Beltramello M, Melchionda S, et al. Pathogenetic role of the deafness-related M34T mutation of Cx26. Hum Mol Genet. 2006;15:2569–2587.
doi: 10.1093/hmg/ddl184
Zonta F, Buratto D, Cassini C, et al. Molecular dynamics simulations highlight structural and functional alterations in deafness-related M34T mutation of connexin 26. Front Physiol. 2014;5:85.
doi: 10.3389/fphys.2014.00085
D’Andrea P, Veronesi V, Bicego M, et al. Hearing loss: frequency and functional studies of the most common connexin26 alleles. Biochem Biophys Res Commun. 2002;296:685–691.
doi: 10.1016/S0006-291X(02)00891-4
de Wolf E, van de Wiel J, Cook J, Dale N Altered CO2 sensitivity of connexin26 mutant hemichannels in vitro. Physiol Rep. 2016;4:e13038;1–12.
Maeda S, Nakagawa S, Suga M, et al. Structure of the connexin 26 gap junction channel at 3.5 A resolution. Nature. 2009;458:597–602.
doi: 10.1038/nature07869
Yilmaz A. Bioinformatic analysis of GJB2 gene missense mutations. Cell Biochem Biophys. 2015;71:1623–1642.
doi: 10.1007/s12013-014-0385-7
Bruzzone R, Veronesi V, Gomes D, et al. Loss-of-function and residual channel activity of connexin26 mutations associated with non-syndromic deafness. FEBS Lett. 2003;533:79–88.
doi: 10.1016/S0014-5793(02)03755-9
Kim J, Jung J, Lee MG, et al. Non-syndromic hearing loss caused by the dominant cis mutation R75Q with the recessive mutation V37I of the GJB2 (Connexin 26) gene. Exp Mol Med. 2015;47:e169.
doi: 10.1038/emm.2015.32
Chen Y, Hu L, Wang X, et al. Characterization of a knock-in mouse model of the homozygous p.V37I variant in Gjb2. Sci Rep. 2016;6:33279.
doi: 10.1038/srep33279
Chan DK, Chang KW. GJB2-associated hearing loss: systematic review of worldwide prevalence, genotype, and auditory phenotype. Laryngoscope. 2014;124:E34–53.
doi: 10.1002/lary.24332
Lameiras AR, Goncalves AC, Santos R, et al. The controversial p.Met34Thr variant in GJB2 gene: two siblings, one genotype, two phenotypes. Int J Pediatr Otorhinolaryngol. 2015;79:1316–1319.
doi: 10.1016/j.ijporl.2015.05.041
Dai ZY, Sun BC, Huang SS, et al. Correlation analysis of phenotype and genotype of GJB2 in patients with non-syndromic hearing loss in China. Gene. 2015;570:272–276.
doi: 10.1016/j.gene.2015.06.038
Chen K, Sun L, Zong L, et al. GJB2 and mitochondrial 12S rRNA susceptibility mutations in sudden deafness. Eur Arch Otorhinolaryngol. 2016;273:1393–1398.
doi: 10.1007/s00405-015-3693-7
Lim LH, Bradshaw JK, Guo Y, et al. Genotypic and phenotypic correlations of DFNB1-related hearing impairment in the Midwestern United States. Arch Otolaryngol Head Neck Surg. 2003;129:836–840.
doi: 10.1001/archotol.129.8.836
Lee KH, Larson DA, Shott G, et al. Audiologic and temporal bone imaging findings in patients with sensorineural hearing loss and GJB2 mutations. Laryngoscope. 2009;119:554–558.
doi: 10.1002/lary.20162
Kenna MA, Feldman HA, Neault MW, et al. Audiologic phenotype and progression in GJB2 (Connexin 26) hearing loss. Arch Otolaryngol Head Neck Surg. 2010;136:81–87.
doi: 10.1001/archoto.2009.202
Jiang Y, Huang S, Deng T, et al. Mutation spectrum of common deafness-causing genes in patients with non-syndromic deafness in the Xiamen Area, China. PLoS ONE. 2015;10:e0135088.
doi: 10.1371/journal.pone.0135088
Zoll B, Petersen L, Lange K, et al. Evaluation of Cx26/GJB2 in German hearing impaired persons: mutation spectrum and detection of disequilibrium between M34T (c.101T>C) and -493del10. Hum Mutat. 2003;21:98.
doi: 10.1002/humu.9098

Auteurs

Jun Shen (J)

Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA. jshen5@bwh.harvard.edu.
Harvard Medical School Center for Hereditary Deafness, Boston, MA, USA. jshen5@bwh.harvard.edu.
Laboratory for Molecular Medicine, Partners HealthCare Personalized Medicine, Cambridge, MA, USA. jshen5@bwh.harvard.edu.

Andrea M Oza (AM)

Laboratory for Molecular Medicine, Partners HealthCare Personalized Medicine, Cambridge, MA, USA.
Department of Otolaryngology and Communication Enhancement, Boston Children's Hospital, Harvard Medical School, Boston, MA, USA.

Ignacio Del Castillo (I)

Servicio de Genetica, Hospital Universitario Ramon y Cajal, IRYCIS, Madrid, Spain.
Centro de Investigacion Biomedica en Red de Enfermedades Raras (CIBERER), Madrid, Spain.

Hatice Duzkale (H)

Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.

Tatsuo Matsunaga (T)

Division of Hearing and Balance Research, National Institute of Sensory Organs, National Hospital Organization Tokyo Medical Center, Tokyo, Japan.

Arti Pandya (A)

University of North Carolina, Chapel Hill, NC, USA.

Hyunseok P Kang (HP)

Counsyl, South San Francisco, CA, USA.

Rebecca Mar-Heyming (R)

Counsyl, South San Francisco, CA, USA.

Saurav Guha (S)

Counsyl, South San Francisco, CA, USA.
New York Genome Center, New York, NY, 10013, USA.

Krista Moyer (K)

Counsyl, South San Francisco, CA, USA.

Christine Lo (C)

Counsyl, South San Francisco, CA, USA.

Margaret Kenna (M)

Harvard Medical School Center for Hereditary Deafness, Boston, MA, USA.
Department of Otolaryngology and Communication Enhancement, Boston Children's Hospital, Harvard Medical School, Boston, MA, USA.

John J Alexander (JJ)

EGL Genetics/Department of Human Genetics, Emory University School of Medicine, Atlanta, GA, USA.
ConsulGene, LLC, Jacksonville, FL, USA.

Yan Zhang (Y)

Certer for Medical Genetics, Guangdong Women and Children Hospital, Guangzhou, Guangdong, China.

Yoel Hirsch (Y)

Dor Yeshorim, Committee for Prevention of Jewish Genetic Diseases, Brooklyn, NY, USA.

Minjie Luo (M)

The Children's Hospital of Philadelphia, Philadelphia, PA, USA.
The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, USA.

Ye Cao (Y)

Department of Obstetrics and Gynecology, The Chinese University of Hong Kong, Hong Kong, China.

Kwong Wai Choy (K)

Department of Obstetrics and Gynecology, The Chinese University of Hong Kong, Hong Kong, China.

Yen-Fu Cheng (YF)

Department of Medical Research, Taipei Veterans General Hospital, Taipei, Taiwan.
Department of Otolaryngology-Head and Neck Surgery, Taipei Veterinary Hospital, Taipei, Taiwan.
School of Medicine, National Yang-Ming University, Taipei, Taiwan.

Karen B Avraham (KB)

Raphael Recanati Genetic Institute, Rabin Medical Center-Beilinson Hospital, Petach Tikva, Israel.

Xinhua Hu (X)

Department of Biostatistics, Fairbanks School of Public Health and School of Medicine, Indiana University, Indianapolis, IN, USA.

Gema Garrido (G)

Servicio de Genetica, Hospital Universitario Ramon y Cajal, IRYCIS, Madrid, Spain.
Centro de Investigacion Biomedica en Red de Enfermedades Raras (CIBERER), Madrid, Spain.

Miguel A Moreno-Pelayo (MA)

Servicio de Genetica, Hospital Universitario Ramon y Cajal, IRYCIS, Madrid, Spain.
Centro de Investigacion Biomedica en Red de Enfermedades Raras (CIBERER), Madrid, Spain.

John Greinwald (J)

Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.

Kejian Zhang (K)

Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.

Yukun Zeng (Y)

Certer for Medical Genetics, Guangdong Women and Children Hospital, Guangzhou, Guangdong, China.

Zippora Brownstein (Z)

Raphael Recanati Genetic Institute, Rabin Medical Center-Beilinson Hospital, Petach Tikva, Israel.

Lina Basel-Salmon (L)

Raphael Recanati Genetic Institute, Rabin Medical Center-Beilinson Hospital, Petach Tikva, Israel.
Pediatric Genetics Clinic, Schneider Children's Medical Center of Israel, Petach Tikva, Israel.
Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.
Felsenstein Medical Research Center, Petach Tikva, Israel.

Bella Davidov (B)

Raphael Recanati Genetic Institute, Rabin Medical Center-Beilinson Hospital, Petach Tikva, Israel.

Moshe Frydman (M)

Raphael Recanati Genetic Institute, Rabin Medical Center-Beilinson Hospital, Petach Tikva, Israel.
Danek Gartner Institute of Human Genetics, Sheba Medical Center, Tel Hashomer, Israel.

Tzvi Weiden (T)

Dor Yeshorim, Committee for Prevention of Jewish Genetic Diseases, Jerusalem, Israel.

Narasimhan Nagan (N)

Integrated Genetics, Laboratory Corporation of America® Holdings, Westborough, MA, USA.

Alecia Willis (A)

Integrated Genetics, Laboratory Corporation of America® Holdings, Research Triangle Park, NC, USA.

Sarah E Hemphill (SE)

Laboratory for Molecular Medicine, Partners HealthCare Personalized Medicine, Cambridge, MA, USA.

Andrew R Grant (AR)

Laboratory for Molecular Medicine, Partners HealthCare Personalized Medicine, Cambridge, MA, USA.
The Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Rebecca K Siegert (RK)

Laboratory for Molecular Medicine, Partners HealthCare Personalized Medicine, Cambridge, MA, USA.
The Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Marina T DiStefano (MT)

Laboratory for Molecular Medicine, Partners HealthCare Personalized Medicine, Cambridge, MA, USA.

Sami S Amr (SS)

Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Harvard Medical School Center for Hereditary Deafness, Boston, MA, USA.
Laboratory for Molecular Medicine, Partners HealthCare Personalized Medicine, Cambridge, MA, USA.

Heidi L Rehm (HL)

Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Harvard Medical School Center for Hereditary Deafness, Boston, MA, USA.
Laboratory for Molecular Medicine, Partners HealthCare Personalized Medicine, Cambridge, MA, USA.
The Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.

Ahmad N Abou Tayoun (AN)

Al Jalila Children's Specialty Hospital, Dubai, UAE. Ahmad.Tayoun@ajch.ae.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH