A relatively common homozygous TRAPPC4 splicing variant is associated with an early-infantile neurodegenerative syndrome.


Journal

European journal of human genetics : EJHG
ISSN: 1476-5438
Titre abrégé: Eur J Hum Genet
Pays: England
ID NLM: 9302235

Informations de publication

Date de publication:
02 2021
Historique:
received: 10 05 2020
accepted: 21 08 2020
revised: 01 08 2020
pubmed: 10 9 2020
medline: 19 1 2022
entrez: 9 9 2020
Statut: ppublish

Résumé

Trafficking protein particle (TRAPP) complexes, which include the TRAPPC4 protein, regulate membrane trafficking between lipid organelles in a process termed vesicular tethering. TRAPPC4 was recently implicated in a recessive neurodevelopmental condition in four unrelated families due to a shared c.454+3A>G splice variant. Here, we report 23 patients from 17 independent families with an early-infantile-onset neurodegenerative presentation, where we also identified the homozygous variant hg38:11:119020256 A>G (NM_016146.5:c.454+3A>G) in TRAPPC4 through exome or genome sequencing. No other clinically relevant TRAPPC4 variants were identified among any of over 10,000 patients with neurodevelopmental conditions. We found the carrier frequency of TRAPPC4 c.454+3A>G was 2.4-5.4 per 10,000 healthy individuals. Affected individuals with the homozygous TRAPPC4 c.454+3A>G variant showed profound psychomotor delay, developmental regression, early-onset epilepsy, microcephaly and progressive spastic tetraplegia. Based upon RNA sequencing, the variant resulted in partial exon 3 skipping and generation of an aberrant transcript owing to use of a downstream cryptic splice donor site, predicting a premature stop codon and nonsense mediated decay. These data confirm the pathogenicity of the TRAPPC4 c.454+3A>G variant, and refine the clinical presentation of TRAPPC4-related encephalopathy.

Identifiants

pubmed: 32901138
doi: 10.1038/s41431-020-00717-5
pii: 10.1038/s41431-020-00717-5
pmc: PMC7868361
doi:

Substances chimiques

Codon, Nonsense 0
Nerve Tissue Proteins 0
RNA Splice Sites 0
TRAPPC4 protein, human 0
Vesicular Transport Proteins 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

271-279

Subventions

Organisme : NHGRI NIH HHS
ID : UM1 HG008900
Pays : United States
Organisme : NHGRI NIH HHS
ID : R01 HG009141
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001863
Pays : United States
Organisme : Department of Health
Pays : United Kingdom
Organisme : NINDS NIH HHS
ID : R01 NS098004
Pays : United States
Organisme : NHGRI NIH HHS
ID : UM1 HG006504
Pays : United States
Organisme : NHGRI NIH HHS
ID : U01 HG007672
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS048453
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM008666
Pays : United States
Organisme : Medical Research Council
ID : G0601943
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/S01165X/1
Pays : United Kingdom
Organisme : NINDS NIH HHS
ID : R01 NS106387
Pays : United States
Organisme : Medical Research Council
ID : MR/S005021/1
Pays : United Kingdom
Organisme : NICHD NIH HHS
ID : F31 HD095602
Pays : United States

Références

Brunet S, Sacher M. In sickness and in health: the role of TRAPP and associated proteins in disease. Traffic. 2014;8:803–18.
doi: 10.1111/tra.12183
Milev MP, Graziano C, Karall D, Kuper WFE, AL-Deri N, Cordelli DM, et al. Bi-allelic mutations in TRAPPC2L result in a neurodevelopmental disorder and have an impact on RAB11 in fibroblasts. J Med Genet. 2018;55:753–64.
doi: 10.1136/jmedgenet-2018-105441
Gedeon AK, Colley A, Jamieson R, Thompson EM, Rogers J, Sillence D, et al. Identification of the gene (SEDL) causing X-linked spondyloepiphyseal dysplasia tarda. Nat Genet. 1999;22:400–4.
doi: 10.1038/11976
Bogershausen N, Shahrzad N, Chong JX, von Kleist-Retzow JC, Stanga D, Li Y, et al. Recessive TRAPPC11 mutations cause a disease spectrum of limb girdle muscular dystrophy and myopathy with movement disorder and intellectual disability. Am J Hum Genet. 2013;93:181–90.
doi: 10.1016/j.ajhg.2013.05.028
Marin-Valencia I, Novarino G, Johansen A, Rosti B, Issa MY, Musaev D, et al. A homozygous founder mutation in TRAPPC6B associates with a neurodevelopmental disorder characterised by microcephaly, epilepsy and autistic features. J Med Genet. 2018;55:48–54.
doi: 10.1136/jmedgenet-2017-104627
Sacher M, Shahrzad N, Kamel H. TRAPPopathies: an emerging set of disorders linked to variations in the genes encoding transport protein particle (TRAPP)-associated proteins. Traffic. 2019;1:5–26.
doi: 10.1111/tra.12615
Van Bergen NJ, Guo Y, Al-Deri N, Lipatova Z, Stanga D, Zhao S, et al. Deficiencies in vesicular transport mediated by TRAPPC4 are associated with severe syndromic intellectual disability. Brain. 2019;143:112–30.
doi: 10.1093/brain/awz374
Kaur P, Kadavigere R, Girisha KM, Shukla A. Recurrent bi-allelic splicing variant c.454+3A>G in TRAPPC4 is associated with progressive encephalopathy and muscle involvement. Brain. 2020;143:e29.
pubmed: 32125366
Yang Y, Muzny DM, Reid JG, Bainbridge MN, Willis A, Ward PA, et al. Clinical whole-exome sequencing for the diagnosis of Mendelian disorders. N Engl J Med. 2013;16:1502–11.
doi: 10.1056/NEJMoa1306555
Bauer P, Kandaswamy KK, Weiss MER, Paknia O, Werber M, Bertoli-Avella AM, et al. Development of an evidence-based algorithm that optimizes sensitivity and specificity in ES-based diagnostics of a clinically heterogeneous patient population. Genet Med. 2019;1:53–61.
doi: 10.1038/s41436-018-0016-6
Retterer K, Juusola J, Cho MT, Vitazka P, Millan F, Gibellini F, et al. Clinical application of whole-exome sequencing across clinical indications. Genet Med. 2016;7:696–704.
doi: 10.1038/gim.2015.148
Sadedin SP, Pope B, Oshlack A. Bpipe: a tool for running and managing bioinformatics pipelines. Bioinformatics. 2012;11:1525–6.
doi: 10.1093/bioinformatics/bts167
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;15:2114–20.
doi: 10.1093/bioinformatics/btu170
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;1:15–21.
doi: 10.1093/bioinformatics/bts635
Liao Y, Smyth GK, Shi W. The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads. Nucleic Acids Res. 2019;8:e47.
doi: 10.1093/nar/gkz114
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
doi: 10.1186/s13059-014-0550-8
Garrido-Martin D, Palumbo E, Guigo R, Breschi A. ggsashimi: Sashimi plot revised for browser- and annotation-independent splicing visualization. PLoS Comput Biol. 2018;8:e1006360.
doi: 10.1371/journal.pcbi.1006360
Dixon-Salazar TJ, Silhavy JL, Udpa N, Schroth J, Bielas S, Schaffer AE, et al. Exome sequencing can improve diagnosis and alter patient management. Sci Transl Med. 2012;4:138ra78.
doi: 10.1126/scitranslmed.3003544
Scott EM, Halees A, Itan Y, Spencer EG, He Y, Azab MA, et al. Characterization of Greater Middle Eastern genetic variation for enhanced disease gene discovery. Nat Genet. 2016;48:1071–6.
doi: 10.1038/ng.3592
Gonorazky HD, Naumenko S, Ramani AK, Nelakuditi V, Mashouri P, Wang P, et al. Expanding the boundaries of RNA sequencing as a diagnostic tool for rare Mendelian disease. Am J Hum Genet. 2019;104:466–83.
doi: 10.1016/j.ajhg.2019.01.012

Auteurs

Shereen G Ghosh (SG)

Department of Neurosciences, University of California, San Diego, La Jolla, CA, 92093, USA.
Rady Children's Institute for Genomic Medicine, San Diego, CA, 92025, USA.

Marcello Scala (M)

Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genoa, Genoa, Italy.
Department of Neuromuscular Disorders, Queen Square Institute of Neurology, University College London, WC1N 3BG, London, UK.

Christian Beetz (C)

CENTOGENE AG, Rostock, Germany.

Guy Helman (G)

Murdoch Children's Research Institute, Royal Children's Hospital, Parkville, VIC, Australia.
Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, Australia.

Valentina Stanley (V)

Department of Neurosciences, University of California, San Diego, La Jolla, CA, 92093, USA.
Rady Children's Institute for Genomic Medicine, San Diego, CA, 92025, USA.

Xiaoxu Yang (X)

Department of Neurosciences, University of California, San Diego, La Jolla, CA, 92093, USA.
Rady Children's Institute for Genomic Medicine, San Diego, CA, 92025, USA.

Martin W Breuss (MW)

Department of Neurosciences, University of California, San Diego, La Jolla, CA, 92093, USA.
Rady Children's Institute for Genomic Medicine, San Diego, CA, 92025, USA.

Neda Mazaheri (N)

Department of Genetics, Shahid Chamran University of Ahvaz, Ahvaz, Iran.

Laila Selim (L)

Division of Neurology and Metabolism, Kasr Al Ainy School of Medicine, Cairo University Children Hospital, Cairo, Egypt.

Fatemeh Hadipour (F)

Department of Medical Genetics, Atieh Hospital, Tehran, Iran.

Lynn Pais (L)

Broad Center for Mendelian Genomics, Program in Medical and Population Genetics, Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, MA, 02142, USA.

Chloe A Stutterd (CA)

Murdoch Children's Research Institute, Royal Children's Hospital, Parkville, VIC, Australia.
Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, Australia.
Department of Paediatrics, University of Melbourne, Melbourne, VIC, Australia.

Vasiliki Karageorgou (V)

CENTOGENE AG, Rostock, Germany.

Amber Begtrup (A)

GeneDx, Gaithersburg, MD, USA.

Amy Crunk (A)

GeneDx, Gaithersburg, MD, USA.

Jane Juusola (J)

GeneDx, Gaithersburg, MD, USA.

Rebecca Willaert (R)

GeneDx, Gaithersburg, MD, USA.

Leigh A Flore (LA)

Division of Genetic, Genomic & Metabolic Disorders, Children's Hospital of Michigan, Detroit, MI, USA.

Kelly Kennelly (K)

Division of Genetic, Genomic & Metabolic Disorders, Children's Hospital of Michigan, Detroit, MI, USA.

Christopher Spencer (C)

Division of Pediatric Genetics, Department of Pediatrics, UF College of Medicine, Jacksonville, FL, 32207, USA.

Martha Brown (M)

Division of Pediatric Genetics, Department of Pediatrics, UF College of Medicine, Jacksonville, FL, 32207, USA.

Pamela Trapane (P)

Division of Pediatric Genetics, Department of Pediatrics, UF College of Medicine, Jacksonville, FL, 32207, USA.

Anna C E Hurst (ACE)

Department of Genetics, University of Alabama at Birmingham, Birmingham, AL, USA.

S Lane Rutledge (S)

Department of Genetics, University of Alabama at Birmingham, Birmingham, AL, USA.

Dana H Goodloe (DH)

Department of Genetics, University of Alabama at Birmingham, Birmingham, AL, USA.

Marie T McDonald (MT)

Division of Medical Genetics, Department of Pediatrics, Duke University Medical Center, Durham, NC, USA.

Vandana Shashi (V)

Division of Medical Genetics, Department of Pediatrics, Duke University Medical Center, Durham, NC, USA.

Kelly Schoch (K)

Division of Medical Genetics, Department of Pediatrics, Duke University Medical Center, Durham, NC, USA.

Hoda Tomoum (H)

Department of Pediatrics, Ain Shams University, Cairo, Egypt.

Raghda Zaitoun (R)

Department of Pediatrics, Ain Shams University, Cairo, Egypt.

Zahra Hadipour (Z)

Department of Medical Genetics, Atieh Hospital, Tehran, Iran.

Hamid Galehdari (H)

Department of Genetics, Shahid Chamran University of Ahvaz, Ahvaz, Iran.

Alistair T Pagnamenta (AT)

NIHR Oxford BRC, Wellcome Centre for Human Genetics, University of Oxford, Oxford, UK.

Majid Mojarrad (M)

Department of Medical Genetics, Mashhad University of Medical Sciences, Mashhad, Iran.
Genetic Research Center, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.
Genetic Center of Khorasan Razavi, Mashhad, Iran.

Alireza Sedaghat (A)

Health Research Institute, Diabetes Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran.

Patrícia Dias (P)

Medical Genetics Service, Paediatrics Department, Centro Hospitalar Universitário Lisboa Norte, Hospital de Santa Maria, Lisbon, Portugal.

Sofia Quintas (S)

Neuropaediatrics Unit, Paediatrics Department, Centro Hospitalar Universitário Lisboa Norte, Hospital de Santa Maria, Lisbon, Portugal.

Atiyeh Eslahi (A)

Department of Medical Genetics, Mashhad University of Medical Sciences, Mashhad, Iran.
Student Research Committee, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.

Gholamreza Shariati (G)

Department of Medical Genetics, Faculty of Medicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran.

Peter Bauer (P)

CENTOGENE AG, Rostock, Germany.

Cas Simons (C)

Murdoch Children's Research Institute, Royal Children's Hospital, Parkville, VIC, Australia.
Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, Australia.

Henry Houlden (H)

Department of Neuromuscular Disorders, Queen Square Institute of Neurology, University College London, WC1N 3BG, London, UK.

Mahmoud Y Issa (MY)

Clinical Genetics Department, Human Genetics and Genome Research Division, National Research Centre, Cairo, Egypt.

Maha S Zaki (MS)

Clinical Genetics Department, Human Genetics and Genome Research Division, National Research Centre, Cairo, Egypt.

Reza Maroofian (R)

Department of Neuromuscular Disorders, Queen Square Institute of Neurology, University College London, WC1N 3BG, London, UK. r.maroofian@ucl.ac.uk.

Joseph G Gleeson (JG)

Department of Neurosciences, University of California, San Diego, La Jolla, CA, 92093, USA. jogleeson@ucsd.edu.
Rady Children's Institute for Genomic Medicine, San Diego, CA, 92025, USA. jogleeson@ucsd.edu.

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