Damaging de novo missense variants in EEF1A2 lead to a developmental and degenerative epileptic-dyskinetic encephalopathy.


Journal

Human mutation
ISSN: 1098-1004
Titre abrégé: Hum Mutat
Pays: United States
ID NLM: 9215429

Informations de publication

Date de publication:
07 2020
Historique:
received: 18 09 2019
revised: 14 02 2020
accepted: 13 03 2020
pubmed: 21 3 2020
medline: 6 11 2021
entrez: 21 3 2020
Statut: ppublish

Résumé

Heterozygous de novo variants in the eukaryotic elongation factor EEF1A2 have previously been described in association with intellectual disability and epilepsy but never functionally validated. Here we report 14 new individuals with heterozygous EEF1A2 variants. We functionally validate multiple variants as protein-damaging using heterologous expression and complementation analysis. Our findings allow us to confirm multiple variants as pathogenic and broaden the phenotypic spectrum to include dystonia/choreoathetosis, and in some cases a degenerative course with cerebral and cerebellar atrophy. Pathogenic variants appear to act via a haploinsufficiency mechanism, disrupting both the protein synthesis and integrated stress response functions of EEF1A2. Our studies provide evidence that EEF1A2 is highly intolerant to variation and that de novo pathogenic variants lead to an epileptic-dyskinetic encephalopathy with both neurodevelopmental and neurodegenerative features. Developmental features may be driven by impaired synaptic protein synthesis during early brain development while progressive symptoms may be linked to an impaired ability to handle cytotoxic stressors.

Identifiants

pubmed: 32196822
doi: 10.1002/humu.24015
pmc: PMC7292794
mid: NIHMS1583672
doi:

Substances chimiques

EEF1A2 protein, human 0
Peptide Elongation Factor 1 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

1263-1279

Subventions

Organisme : NICHD NIH HHS
ID : P50 HD103524
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS106298
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS069605
Pays : United States
Organisme : NINDS NIH HHS
ID : R00 NS089858
Pays : United States

Informations de copyright

© 2020 Wiley Periodicals, Inc.

Références

Genet Med. 2015 Jul;17(7):578-86
pubmed: 25356970
Mol Genet Genomic Med. 2016 Apr 03;4(4):465-74
pubmed: 27441201
J Cell Sci. 2013 Apr 15;126(Pt 8):1744-52
pubmed: 23444377
Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W382-8
pubmed: 15980494
Nature. 2016 Aug 17;536(7616):285-91
pubmed: 27535533
J Med Genet. 2016 Mar;53(3):190-9
pubmed: 26740508
N Engl J Med. 2012 Nov 15;367(20):1921-9
pubmed: 23033978
J Biochem. 2006 Sep;140(3):393-9
pubmed: 16877446
Am J Hum Genet. 2016 Jun 2;98(6):1249-1255
pubmed: 27236917
Clin Genet. 2015 Apr;87(4):356-61
pubmed: 24697219
J Biol Chem. 2003 Oct 31;278(44):43443-51
pubmed: 12920118
Yeast. 2000 Apr;16(6):553-60
pubmed: 10790693
Mol Cell Biol. 2007 Mar;27(5):1974-89
pubmed: 17178834
PLoS One. 2009 Jul 28;4(7):e6315
pubmed: 19636410
Am J Hum Genet. 2019 Aug 1;105(2):267-282
pubmed: 31327507
Science. 2016 Jan 29;351(6272):aad3867
pubmed: 26823435
J Biol Chem. 1992 Jan 15;267(2):699-702
pubmed: 1730661
Mol Cell. 2010 Oct 22;40(2):280-93
pubmed: 20965422
Epilepsia. 2013 Jul;54(7):1270-81
pubmed: 23647072
J Cell Sci. 2016 Dec 15;129(24):4521-4533
pubmed: 27852836
Sci Signal. 2015 Mar 10;8(367):ra27
pubmed: 25759478
PLoS Genet. 2013;9(8):e1003709
pubmed: 23990802
Nucleic Acids Res. 2014 Nov 10;42(20):12939-48
pubmed: 25326326
Mol Cell Biol. 2005 Jan;25(1):403-13
pubmed: 15601860
J Biol Chem. 2011 Oct 21;286(42):36568-79
pubmed: 21849502
Gene. 1995 Apr 14;156(1):119-22
pubmed: 7737504
Sci Rep. 2017 Apr 05;7:46019
pubmed: 28378778
J Mol Biol. 1999 Dec 17;294(5):1351-62
pubmed: 10600390
J Bacteriol. 1983 Jan;153(1):163-8
pubmed: 6336730
Wiley Interdiscip Rev RNA. 2012 Jul-Aug;3(4):543-55
pubmed: 22555874
Genet Med. 2015 May;17(5):405-24
pubmed: 25741868
Epilepsia. 2017 Apr;58(4):512-521
pubmed: 28276062
Int J Biochem Cell Biol. 2004 Jul;36(7):1341-7
pubmed: 15109577
Brain Dev. 2016 May;38(5):520-4
pubmed: 26682508
Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4463-8
pubmed: 9539760
J Biol Chem. 2007 Sep 28;282(39):28951-9
pubmed: 17640869
Methods Enzymol. 2008;451:89-107
pubmed: 19185716
Eur J Biochem. 1993 Aug 1;215(3):549-54
pubmed: 8354261
Nat Genet. 2013 Jul;45(7):825-30
pubmed: 23708187
Cell Rep. 2013 Nov 14;5(3):727-37
pubmed: 24209753
J Biol Chem. 2014 Jul 25;289(30):20928-38
pubmed: 24936063
Curr Genet. 1985;9(8):693-7
pubmed: 3916735
Yeast. 1999 Oct;15(14):1541-53
pubmed: 10514571
Elife. 2014 Sep 16;3:e03164
pubmed: 25233275
Brain Res Dev Brain Res. 2004 Mar 22;149(1):1-8
pubmed: 15013623
NPJ Genom Med. 2018 Aug 13;3:22
pubmed: 30109124
Nat Commun. 2014 Nov 24;5:5595
pubmed: 25418537
Hum Mol Genet. 2017 Sep 15;26(18):3545-3552
pubmed: 28911200

Auteurs

Gemma L Carvill (GL)

Ken and Ruth Davee Department of Neurology, Northwestern University, Chicago, Illinois.

Katherine L Helbig (KL)

Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania.
The Epilepsy NeuroGenetics Initiative, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania.

Candace T Myers (CT)

Division of Genetic Medicine, Department of Pediatrics, Seattle, Washington.

Marcello Scala (M)

Department of Pediatric Neurology & Muscular Disorders, IRCCS Istituto Giannina Gaslini, Via Gerolamo Gaslini, Genoa, Italy.
Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, Università degli Studi di Genova, Genoa, Italy.

Robert Huether (R)

Division of Clinical Genomics, Ambry Genetics, Aliso Viejo, California.

Sara Lewis (S)

Barrow Neurological Institute, Department of Neurology, Phoenix Children's Hospital, Phoenix, Arizona.
Departments of Child Health, Cellular & Molecular Medicine, and Neurology and Program in Genetics, University of Arizona College of Medicine Phoenix, Phoenix, Arizona.

Tyler N Kruer (TN)

Barrow Neurological Institute, Department of Neurology, Phoenix Children's Hospital, Phoenix, Arizona.
Departments of Child Health, Cellular & Molecular Medicine, and Neurology and Program in Genetics, University of Arizona College of Medicine Phoenix, Phoenix, Arizona.

Brandon S Guida (BS)

Barrow Neurological Institute, Department of Neurology, Phoenix Children's Hospital, Phoenix, Arizona.
Departments of Child Health, Cellular & Molecular Medicine, and Neurology and Program in Genetics, University of Arizona College of Medicine Phoenix, Phoenix, Arizona.

Somayeh Bakhtiari (S)

Barrow Neurological Institute, Department of Neurology, Phoenix Children's Hospital, Phoenix, Arizona.
Departments of Child Health, Cellular & Molecular Medicine, and Neurology and Program in Genetics, University of Arizona College of Medicine Phoenix, Phoenix, Arizona.

Joy Sebe (J)

Department of Biology, University of Washington, Seattle, Washington.
Department of Biological Structure, University of Washington, Seattle, Washington.

Sha Tang (S)

Division of Clinical Genomics, Ambry Genetics, Aliso Viejo, California.

Heather Stickney (H)

Department of Biological Structure, University of Washington, Seattle, Washington.

Sehribani Ulusoy Oktay (SU)

Department of Biology, University of Washington, Seattle, Washington.
Department of Biological Structure, University of Washington, Seattle, Washington.

Ashwin A Bhandiwad (AA)

Department of Biological Structure, University of Washington, Seattle, Washington.

Keri Ramsey (K)

Center for Rare Childhood Disorders, Translational Genomics Research Institute, Phoenix, Arizona.

Vinodh Narayanan (V)

Center for Rare Childhood Disorders, Translational Genomics Research Institute, Phoenix, Arizona.

Timothy Feyma (T)

Department of Neurology, Gillette Children's Specialty Healthcare, St. Paul, Minnesota.

Luis O Rohena (LO)

Department of Pediatrics, Division of Genetics, San Antonio Military Medical Center, San Antonio, Texas.
Department of Pediatrics, Long School of Medicine, University of Texas, San Antonio, Texas.

Andrea Accogli (A)

Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, Università degli Studi di Genova, Genoa, Italy.
Medical Genetics Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Mariasavina Severino (M)

Department of Pediatric Neurology & Muscular Disorders, IRCCS Istituto Giannina Gaslini, Via Gerolamo Gaslini, Genoa, Italy.

Georgina Hollingsworth (G)

Departments of Medicine and Paediatrics, University of Melbourne and Austin Health Royal Children's Hospital, Melbourne, Australia.

Deepak Gill (D)

Ty Nelson Department of Neurology, The Children's Hospital at Westmead, Sydney, New South Wales, Australia.

Christel Depienne (C)

INSERM UMR 975, Institut du Cerveau et de la Moelle Epinière, Hôpital Pitié-Salpêtrière, Paris, France.

Caroline Nava (C)

INSERM UMR 975, Institut du Cerveau et de la Moelle Epinière, Hôpital Pitié-Salpêtrière, Paris, France.

Lynette G Sadleir (LG)

Department of Paediatrics and Child Health, University of Otago Wellington, Wellington South, New Zealand.

Paul A Caruso (PA)

Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Boston.

Angela E Lin (AE)

Medical Genetics, Department of Pediatrics, MassGeneral Hospital for Children, Harvard Medical School, Boston, Massachusetts.

Floor E Jansen (FE)

Department of Pediatric Neurology, University Medical Center, Utrecht, The Netherlands.

Bobby Koeleman (B)

Department of Pediatric Neurology, University Medical Center, Utrecht, The Netherlands.

Eva Brilstra (E)

Department of Genetics, Utrecht University, Utrecht, The Netherlands.

Marjolein H Willemsen (MH)

Department of Human Genetics, Radboud University Medical Center, Nijmegen, The Netherlands.

Tjitske Kleefstra (T)

Department of Human Genetics, Radboud University Medical Center, Nijmegen, The Netherlands.

Joaquim Sa (J)

Serviço de Genética Médica, Centro Hospitalar e Universitário de Coimbra, Coimbra, Portugal.

Marie-Laure Mathieu (ML)

Neuropaediatrics Department, Femme Mère Enfant Hospital, Lyon, France.
Claude Bernard Lyon 1 University, Lyon, France.

Laurine Perrin (L)

Department of Paediatric Physical Medicine and Rehabilitation, CHU Saint-Etienne, Hôpital Bellevue, Saint-Étienne, France.

Gaetan Lesca (G)

CRNL Inserm U1028-CNRS UMR5292-Claude Bernard University Lyon 1, Lyon, France.
Department of Medical Genetics, Lyon University Hospital, Lyon, France.

Pasquale Striano (P)

Department of Pediatric Neurology & Muscular Disorders, IRCCS Istituto Giannina Gaslini, Via Gerolamo Gaslini, Genoa, Italy.
Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, Università degli Studi di Genova, Genoa, Italy.

Giorgio Casari (G)

Department of Pediatric Neurology & Muscular Disorders, IRCCS Istituto Giannina Gaslini, Via Gerolamo Gaslini, Genoa, Italy.
Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, Università degli Studi di Genova, Genoa, Italy.

Ingrid E Scheffer (IE)

Departments of Medicine and Paediatrics, University of Melbourne and Austin Health Royal Children's Hospital, Melbourne, Australia.

David Raible (D)

Department of Biology, University of Washington, Seattle, Washington.
Department of Biological Structure, University of Washington, Seattle, Washington.

Evelyn Sattlegger (E)

School of Natural & Computational Sciences, Massey University, Auckland, New Zealand.

Valeria Capra (V)

Department of Pediatric Neurology & Muscular Disorders, IRCCS Istituto Giannina Gaslini, Via Gerolamo Gaslini, Genoa, Italy.

Sergio Padilla-Lopez (S)

Barrow Neurological Institute, Department of Neurology, Phoenix Children's Hospital, Phoenix, Arizona.
Departments of Child Health, Cellular & Molecular Medicine, and Neurology and Program in Genetics, University of Arizona College of Medicine Phoenix, Phoenix, Arizona.

Heather C Mefford (HC)

Division of Genetic Medicine, Department of Pediatrics, Seattle, Washington.

Michael C Kruer (MC)

Barrow Neurological Institute, Department of Neurology, Phoenix Children's Hospital, Phoenix, Arizona.
Departments of Child Health, Cellular & Molecular Medicine, and Neurology and Program in Genetics, University of Arizona College of Medicine Phoenix, Phoenix, Arizona.

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