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December 2021; 7 (6) ArticleOpen Access

Dominant Distal Myopathy 3 (MPD3) Caused by a Deletion in the HNRNPA1 Gene

View ORCID ProfilePeter Hackman, View ORCID ProfileSalla M. Rusanen, View ORCID ProfileMridul Johari, View ORCID ProfileAnna Vihola, View ORCID ProfilePer Harald Jonson, View ORCID ProfileJaakko Sarparanta, View ORCID ProfileKati Donner, Päivi Lahermo, Sampo Koivunen, Helena Luque, Merja Soininen, View ORCID ProfileIbrahim Mahjneh, View ORCID ProfileMari Auranen, View ORCID ProfileMeharji Arumilli, View ORCID ProfileMarco Savarese, View ORCID ProfileBjarne Udd
First published October 27, 2021, DOI: https://doi.org/10.1212/NXG.0000000000000632
Peter Hackman
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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  • ORCID record for Peter Hackman
Salla M. Rusanen
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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  • ORCID record for Salla M. Rusanen
  • For correspondence: salla.valipakka@helsinki.fi
Mridul Johari
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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  • For correspondence: mridul.johari@helsinki.fi
Anna Vihola
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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Per Harald Jonson
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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Jaakko Sarparanta
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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Kati Donner
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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  • For correspondence: kati.donner@helsinki.fi
Päivi Lahermo
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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Sampo Koivunen
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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Helena Luque
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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Merja Soininen
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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Ibrahim Mahjneh
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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  • For correspondence: ibrahim.mahjneh@jakobstad.fi
Mari Auranen
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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  • For correspondence: mari.auranen@hus.fi
Meharji Arumilli
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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Marco Savarese
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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  • For correspondence: marco.savarese@helsinki.fi
Bjarne Udd
From the Folkhälsan Research Center (P.H., S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S., B.U.); University of Helsinki (S.M.R., M.J., A.V., P.H.J., J.S., S.K., H.L., M.S., M.A., M.S.), Helsinki; Finnish Neuromuscular Center, Fimlab Laboratories and Tampere University (A.V.); Institute for Molecular Medicine Finland (FIMM), University of Helsinki (K.D., P.L.); MRC, University of Oulu, Oulu (I.M.); Pietarsaari Hospital, Pietarsaari, Finland (I.M.); Clinical Neurosciences, Neurology, Helsinki University Hospital (M.A.); Vaasa Central Hospital (B.U.), Vaasa, Finland.
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Citation
Dominant Distal Myopathy 3 (MPD3) Caused by a Deletion in the HNRNPA1 Gene
Peter Hackman, Salla M. Rusanen, Mridul Johari, Anna Vihola, Per Harald Jonson, Jaakko Sarparanta, Kati Donner, Päivi Lahermo, Sampo Koivunen, Helena Luque, Merja Soininen, Ibrahim Mahjneh, Mari Auranen, Meharji Arumilli, Marco Savarese, Bjarne Udd
Neurol Genet Dec 2021, 7 (6) e632; DOI: 10.1212/NXG.0000000000000632

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Abstract

Background and Objectives To determine the genetic cause of the disease in the previously reported family with adult-onset autosomal dominant distal myopathy (myopathy, distal, 3; MPD3).

Methods Continued clinical evaluation including muscle MRI and muscle pathology. A linkage analysis with single nucleotide polymorphism arrays and genome sequencing were used to identify the genetic defect, which was verified by Sanger sequencing. RNA sequencing was used to investigate the transcriptional effects of the identified genetic defect.

Results Small hand muscles (intrinsic, thenar, and hypothenar) were first involved with spread to the lower legs and later proximal muscles. Dystrophic changes with rimmed vacuoles and cytoplasmic inclusions were observed in muscle biopsies at advanced stage. A single nucleotide polymorphism array confirmed the previous microsatellite-based linkage to 8p22-q11 and 12q13-q22. Genome sequencing of three affected family members combined with structural variant calling revealed a small heterozygous deletion of 160 base pairs spanning the second last exon 10 of the heterogeneous nuclear ribonucleoprotein A1 (HNRNPA1) gene, which is in the linked region on chromosome 12. Segregation of the mutation with the disease was confirmed by Sanger sequencing. RNA sequencing showed that the mutant allele produces a shorter mutant mRNA transcript compared with the wild-type allele. Immunofluorescence studies on muscle biopsies revealed small p62 and larger TDP-43 inclusions.

Discussion A small exon 10 deletion in the gene HNRNPA1 was identified as the cause of MPD3 in this family. The new HNRNPA1-related phenotype, upper limb presenting distal myopathy, was thus confirmed, and the family displays the complexities of gene identification.

Glossary

bp=
base pair;
CNV=
copy number variant;
DAFO=
dynamic ankle foot orthosis;
GS=
genome sequencing;
HNRNPA1=
heterogeneous nuclear ribonucleoprotein A1;
LOD=
logarithm of odds;
MPD3=
myopathy, distal, 3;
MSP=
multisystem proteinopathy;
PrLD=
prion-like domain

Footnotes

  • Go to Neurology.org/NG for full disclosures. Funding information is provided at the end of the article.

  • The Article Processing Charge was funded by the University of Helsinki.

  • Received July 21, 2021.
  • Revision received August 27, 2021.
  • Accepted in final form September 8, 2021.
  • Copyright © 2021 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

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