Distinct effects on mRNA export factor GANP underlie neurological disease phenotypes and alter gene expression depending on intron content.


Journal

Human molecular genetics
ISSN: 1460-2083
Titre abrégé: Hum Mol Genet
Pays: England
ID NLM: 9208958

Informations de publication

Date de publication:
03 06 2020
Historique:
received: 29 01 2020
revised: 17 03 2020
accepted: 19 03 2020
pubmed: 24 3 2020
medline: 13 8 2021
entrez: 24 3 2020
Statut: ppublish

Résumé

Defects in the mRNA export scaffold protein GANP, encoded by the MCM3AP gene, cause autosomal recessive early-onset peripheral neuropathy with or without intellectual disability. We extend here the phenotypic range associated with MCM3AP variants, by describing a severely hypotonic child and a sibling pair with a progressive encephalopathic syndrome. In addition, our analysis of skin fibroblasts from affected individuals from seven unrelated families indicates that disease variants result in depletion of GANP except when they alter critical residues in the Sac3 mRNA binding domain. GANP depletion was associated with more severe phenotypes compared with the Sac3 variants. Patient fibroblasts showed transcriptome alterations that suggested intron content-dependent regulation of gene expression. For example, all differentially expressed intronless genes were downregulated, including ATXN7L3B, which couples mRNA export to transcription activation by association with the TREX-2 and SAGA complexes. Our results provide insight into the molecular basis behind genotype-phenotype correlations in MCM3AP-associated disease and suggest mechanisms by which GANP defects might alter RNA metabolism.

Identifiants

pubmed: 32202298
pii: 5810984
doi: 10.1093/hmg/ddaa051
pmc: PMC7297229
mid: EMS86591
doi:

Substances chimiques

ATXN7L3B protein, human 0
Antigens, Surface 0
Flavoproteins 0
Glycoproteins 0
Intracellular Signaling Peptides and Proteins 0
Nuclear Proteins 0
PCID2 protein, human 0
Phosphoproteins 0
RNA, Messenger 0
SAGA-1 protein, human 0
Transcription Factors 0
Acetyltransferases EC 2.3.1.-
MCM3AP protein, human EC 2.3.1.-
Exodeoxyribonucleases EC 3.1.-
TREX2 protein, human EC 3.1.16.-
FIG4 protein, human EC 3.1.3.-
Phosphoric Monoester Hydrolases EC 3.1.3.2

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1426-1439

Subventions

Organisme : Medical Research Council
ID : MC_U105178939
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/K010611/1
Pays : United Kingdom
Organisme : NHGRI NIH HHS
ID : UM1 HG008900
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007748
Pays : United States

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press.

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Auteurs

Rosa Woldegebriel (R)

Stem Cells and Metabolism Research Program, Research Programs Unit, University of Helsinki, 00290 Helsinki, Finland.
Maurice Wohl Clinical Neuroscience Institute, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.

Jouni Kvist (J)

Stem Cells and Metabolism Research Program, Research Programs Unit, University of Helsinki, 00290 Helsinki, Finland.

Noora Andersson (N)

Department of Pathology, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.
Research Program in Systems Oncology, University of Helsinki, Helsinki, Finland.

Katrin Õunap (K)

Department of Clinical Genetics, United Laboratories, Tartu University Hospital, Tartu, Estonia.
Department of Clinical Genetics, Institute of Clinical Medicine, University of Tartu, Tartu, Estonia.

Karit Reinson (K)

Department of Clinical Genetics, United Laboratories, Tartu University Hospital, Tartu, Estonia.
Department of Clinical Genetics, Institute of Clinical Medicine, University of Tartu, Tartu, Estonia.

Monica H Wojcik (MH)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Divisions of Genetics and Genomics and Newborn Medicine, Department of Pediatrics, Boston Children's Hospital, Harvard Medical School, Boston, MA, USA.

Emilia K Bijlsma (EK)

Department of Clinical Genetics, Leiden University Medical Centre, Leiden, the Netherlands.

Mariëtte J V Hoffer (MJV)

Department of Clinical Genetics, Leiden University Medical Centre, Leiden, the Netherlands.

Monique M Ryan (MM)

Murdoch Children's Research Institute, Melbourne 3052, Australia.
Royal Children's Hospital, Melbourne 3052, Australia.
Department of Paediatrics, The University of Melbourne, Melbourne 3052, Australia.

Zornitza Stark (Z)

Murdoch Children's Research Institute, Melbourne 3052, Australia.
Department of Paediatrics, The University of Melbourne, Melbourne 3052, Australia.

Maie Walsh (M)

Murdoch Children's Research Institute, Melbourne 3052, Australia.

Inge Cuppen (I)

Department of Pediatric Neurology, Wilhelmina Children's Hospital, University Medical Center Utrecht, Utrecht, The Netherlands.

Marie-Jose H van den Boogaard (MH)

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

Diana Bharucha-Goebel (D)

Neuromuscular and Neurogenetic Disorders of Childhood Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA.
Division of Neurology, Children's National Health System, Washington, DC, USA.

Sandra Donkervoort (S)

Neuromuscular and Neurogenetic Disorders of Childhood Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA.

Sara Winchester (S)

Child Neurology Center of Northwest Florida, Pensacola, FL, USA.

Roberto Zori (R)

Division of Genetics and Metabolism, University of Florida, Gainesville, FL, USA.

Carsten G Bönnemann (CG)

Neuromuscular and Neurogenetic Disorders of Childhood Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA.

Reza Maroofian (R)

Department of Neuromuscular Disorders, UCL Institute of Neurology, London WC1N 3BG, UK.

Emer O'Connor (E)

Department of Neuromuscular Disorders, UCL Institute of Neurology, London WC1N 3BG, UK.

Henry Houlden (H)

Department of Neuromuscular Disorders, UCL Institute of Neurology, London WC1N 3BG, UK.

Fang Zhao (F)

Department of Pathology and Genetics, HUSLAB Laboratories, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.

Olli Carpén (O)

Department of Pathology, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.
Research Program in Systems Oncology, University of Helsinki, Helsinki, Finland.

Matthew White (M)

Maurice Wohl Clinical Neuroscience Institute, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.

Jemeen Sreedharan (J)

Maurice Wohl Clinical Neuroscience Institute, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.

Murray Stewart (M)

MRC Laboratory of Molecular Biology, Francis Crick Ave, Cambridge Biomedical Campus, Cambridge CB2 0QH, UK.

Emil Ylikallio (E)

Stem Cells and Metabolism Research Program, Research Programs Unit, University of Helsinki, 00290 Helsinki, Finland.
Clinical Neurosciences, Neurology, University of Helsinki and Helsinki University Hospital, 00290 Helsinki, Finland.

Henna Tyynismaa (H)

Stem Cells and Metabolism Research Program, Research Programs Unit, University of Helsinki, 00290 Helsinki, Finland.
Department of Medical and Clinical Genetics, University of Helsinki, 00290 Helsinki, Finland.
Neuroscience Center, Helsinki Institute of Life Science, University of Helsinki, Helsinki, Finland.

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Classifications MeSH