Genotype-phenotype correlations and disease mechanisms in PEX13-related Zellweger spectrum disorders.


Journal

Orphanet journal of rare diseases
ISSN: 1750-1172
Titre abrégé: Orphanet J Rare Dis
Pays: England
ID NLM: 101266602

Informations de publication

Date de publication:
19 07 2022
Historique:
received: 07 02 2022
accepted: 26 06 2022
entrez: 19 7 2022
pubmed: 20 7 2022
medline: 22 7 2022
Statut: epublish

Résumé

Pathogenic variants in PEX-genes can affect peroxisome assembly and function and cause Zellweger spectrum disorders (ZSDs), characterized by variable phenotypes in terms of disease severity, age of onset and clinical presentations. So far, defects in at least 15 PEX-genes have been implicated in Mendelian diseases, but in some of the ultra-rare ZSD subtypes genotype-phenotype correlations and disease mechanisms remain elusive. We report five families carrying biallelic variants in PEX13. The identified variants were initially evaluated by using a combination of computational approaches. Immunofluorescence and complementation studies on patient-derived fibroblasts were performed in two patients to investigate the cellular impact of the identified mutations. Three out of five families carried a recurrent p.Arg294Trp non-synonymous variant. Individuals affected with PEX13-related ZSD presented heterogeneous clinical features, including hypotonia, developmental regression, hearing/vision impairment, progressive spasticity and brain leukodystrophy. Computational predictions highlighted the involvement of the Arg294 residue in PEX13 homodimerization, and the analysis of blind docking predicted that the p.Arg294Trp variant alters the formation of dimers, impairing the stability of the PEX13/PEX14 translocation module. Studies on muscle tissues and patient-derived fibroblasts revealed biochemical alterations of mitochondrial function and identified mislocalized mitochondria and a reduced number of peroxisomes with abnormal PEX13 concentration. This study expands the phenotypic and mutational spectrum of PEX13-related ZSDs and also highlight a variety of disease mechanisms contributing to PEX13-related clinical phenotypes, including the emerging contribution of secondary mitochondrial dysfunction to the pathophysiology of ZSDs.

Sections du résumé

BACKGROUND
Pathogenic variants in PEX-genes can affect peroxisome assembly and function and cause Zellweger spectrum disorders (ZSDs), characterized by variable phenotypes in terms of disease severity, age of onset and clinical presentations. So far, defects in at least 15 PEX-genes have been implicated in Mendelian diseases, but in some of the ultra-rare ZSD subtypes genotype-phenotype correlations and disease mechanisms remain elusive.
METHODS
We report five families carrying biallelic variants in PEX13. The identified variants were initially evaluated by using a combination of computational approaches. Immunofluorescence and complementation studies on patient-derived fibroblasts were performed in two patients to investigate the cellular impact of the identified mutations.
RESULTS
Three out of five families carried a recurrent p.Arg294Trp non-synonymous variant. Individuals affected with PEX13-related ZSD presented heterogeneous clinical features, including hypotonia, developmental regression, hearing/vision impairment, progressive spasticity and brain leukodystrophy. Computational predictions highlighted the involvement of the Arg294 residue in PEX13 homodimerization, and the analysis of blind docking predicted that the p.Arg294Trp variant alters the formation of dimers, impairing the stability of the PEX13/PEX14 translocation module. Studies on muscle tissues and patient-derived fibroblasts revealed biochemical alterations of mitochondrial function and identified mislocalized mitochondria and a reduced number of peroxisomes with abnormal PEX13 concentration.
CONCLUSIONS
This study expands the phenotypic and mutational spectrum of PEX13-related ZSDs and also highlight a variety of disease mechanisms contributing to PEX13-related clinical phenotypes, including the emerging contribution of secondary mitochondrial dysfunction to the pathophysiology of ZSDs.

Identifiants

pubmed: 35854306
doi: 10.1186/s13023-022-02415-5
pii: 10.1186/s13023-022-02415-5
pmc: PMC9295491
doi:

Substances chimiques

Membrane Proteins 0
PEX13 protein, human 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

286

Informations de copyright

© 2022. The Author(s).

Références

Am J Hum Genet. 1999 Sep;65(3):621-34
pubmed: 10441568
Nat Protoc. 2012 May 31;7(6):1235-46
pubmed: 22653162
J Inherit Metab Dis. 2016 Jan;39(1):93-106
pubmed: 26287655
Eur J Pediatr. 2015 Apr;174(4):557-63
pubmed: 25287621
Hum Mol Genet. 1999 Jun;8(6):1077-83
pubmed: 10332040
Science. 1973 Oct 5;182(4107):62-4
pubmed: 4730055
J Med Genet. 2010 Sep;47(9):608-15
pubmed: 20647552
Biochim Biophys Acta. 2006 Dec;1763(12):1585-91
pubmed: 17056133
EMBO Rep. 2021 Oct 5;22(10):e51991
pubmed: 34351705
Proc Jpn Acad Ser B Phys Biol Sci. 2016;92(10):463-477
pubmed: 27941306
EMBO J. 2009 Mar 18;28(6):745-54
pubmed: 19197237
Can J Neurol Sci. 1983 Aug;10(3):170-7
pubmed: 6616347
Nucleic Acids Res. 2018 Jul 2;46(W1):W296-W303
pubmed: 29788355
J Inherit Metab Dis. 2015 Jul;38(4):681-702
pubmed: 25687155
Am J Med Genet A. 2009 Jun;149A(6):1219-23
pubmed: 19449432
J Cell Biol. 1996 Dec;135(6 Pt 2):1763-74
pubmed: 8991089
Top Magn Reson Imaging. 2018 Aug;27(4):241-257
pubmed: 30086110
Clin Genet. 2005 Feb;67(2):107-33
pubmed: 15679822
Biochem Biophys Res Commun. 1998 Feb 13;243(2):368-71
pubmed: 9480815
Pediatr Neurol. 1986 May-Jun;2(3):141-6
pubmed: 3508688
Nat Commun. 2019 Jul 12;10(1):3094
pubmed: 31300657
Bioinformatics. 2013 Apr 1;29(7):845-54
pubmed: 23407358
Biochim Biophys Acta. 2016 May;1863(5):922-33
pubmed: 26611709
Biochim Biophys Acta. 2012 Sep;1822(9):1363-73
pubmed: 22178243
Biochim Biophys Acta. 2012 Sep;1822(9):1489-500
pubmed: 22446031
J Mol Biol. 2016 Feb 22;428(4):720-725
pubmed: 26410586
Orphanet J Rare Dis. 2011 Mar 10;6:8
pubmed: 21392394
Hum Mutat. 2006 Nov;27(11):1157
pubmed: 17041890
Hum Mol Genet. 2013 Oct 1;22(19):3844-57
pubmed: 23716570
Front Cell Dev Biol. 2015 May 27;3:35
pubmed: 26075204
FEBS J. 2019 Jan;286(1):205-222
pubmed: 30414318
Virchows Arch B Cell Pathol Incl Mol Pathol. 1984;45(2):125-38
pubmed: 6143441
Mol Cell. 2002 Nov;10(5):1007-17
pubmed: 12453410
Neuroscience. 2016 Oct 15;334:201-213
pubmed: 27514574
Proteins. 2010 Jun;78(8):1950-8
pubmed: 20408171
J Appl Genet. 2020 Feb;61(1):87-91
pubmed: 31628608

Auteurs

Paola Borgia (P)

Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genoa, 16132, Genoa, Italy.
Pediatric Neurology and Muscular Diseases Unit, IRCCS Giannina Gaslini Institute, 16147, Genoa, Italy.

Simona Baldassari (S)

Unit of Medical Genetics, IRCCS Istituto Giannina Gaslini, 16147, Genoa, Italy.

Nicoletta Pedemonte (N)

Unit of Medical Genetics, IRCCS Istituto Giannina Gaslini, 16147, Genoa, Italy.

Ebba Alkhunaizi (E)

Department of Genetics, North York General Hospital, University of Toronto, Toronto, ON, Canada.

Gianluca D'Onofrio (G)

Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genoa, 16132, Genoa, Italy.
Pediatric Neurology and Muscular Diseases Unit, IRCCS Giannina Gaslini Institute, 16147, Genoa, Italy.

Domenico Tortora (D)

Neuroradiology Unit, IRCCS Istituto Giannina Gaslini, 16147, Genoa, Italy.

Elisa Calì (E)

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

Paolo Scudieri (P)

Unit of Medical Genetics, IRCCS Istituto Giannina Gaslini, 16147, Genoa, Italy.

Ganna Balagura (G)

Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genoa, 16132, Genoa, Italy.

Ilaria Musante (I)

Unit of Medical Genetics, IRCCS Istituto Giannina Gaslini, 16147, Genoa, Italy.

Maria Cristina Diana (MC)

Pediatric Neurology and Muscular Diseases Unit, IRCCS Giannina Gaslini Institute, 16147, Genoa, Italy.

Marina Pedemonte (M)

Pediatric Neurology and Muscular Diseases Unit, IRCCS Giannina Gaslini Institute, 16147, Genoa, Italy.

Maria Stella Vari (MS)

Pediatric Neurology and Muscular Diseases Unit, IRCCS Giannina Gaslini Institute, 16147, Genoa, Italy.

Michele Iacomino (M)

Unit of Medical Genetics, IRCCS Istituto Giannina Gaslini, 16147, Genoa, Italy.

Antonella Riva (A)

Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genoa, 16132, Genoa, Italy.
Pediatric Neurology and Muscular Diseases Unit, IRCCS Giannina Gaslini Institute, 16147, Genoa, Italy.

Roberto Chimenz (R)

Unit of Pediatric Nephrology and Dialysis, Department of Human Pathology in Adult and Developmental Age "Gaetano Barresi", University of Messina, Via Consolare Valeria 1, 98125, Messina, Italy.

Giuseppe D Mangano (GD)

Department Pro.M.I.S.E. "G. D'Alessandro", University of Palermo, Palermo, Italy.

Mohammad Hasan Mohammadi (MH)

Department of Pediatrics, Zabol University of Medical Sciences, Zabol, Iran.

Mehran Beiraghi Toosi (MB)

Pediatric Neurology Department, Ghaem Hospital, Mashhad University of Medical Sciences, Mashhad, Iran.

Farah Ashrafzadeh (F)

Department of Pediatrics, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.

Shima Imannezhad (S)

Pediatric Neurology Department, Ghaem Hospital, Mashhad University of Medical Sciences, Mashhad, Iran.

Ehsan Ghayoor Karimiani (EG)

Molecular and Clinical Sciences Institute, St. George's, University of London, Cranmer Terrace, London, SW170RE, UK.
Innovative Medical Research Center, Mashhad Branch, Islamic Azad University, Mashhad, Iran.

Andrea Accogli (A)

Division of Medical Genetics, Department of Specialized Medicine, Montreal Children's Hospital, McGill University Health Centre (MUHC), Montreal, QC, H4A 3J1, Canada.
Department of Human Genetics, McGill University, Montreal, QC, Canada.

Maria Cristina Schiaffino (MC)

Pediatric Clinic and Endocrinology Unit, Department of General and Specialist Pediatric Sciences, University of Genoa, 16147, Genoa, Italy.

Mohamad Maghnie (M)

Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genoa, 16132, Genoa, Italy.
Pediatric Clinic and Endocrinology Unit, Department of General and Specialist Pediatric Sciences, University of Genoa, 16147, Genoa, Italy.

Miguel Angel Soler (MA)

Computational Modelling of Nanoscale and Biophysical Systems Laboratory, Italian Institute of Technology, 16163, Genoa, Italy.

Karl Echiverri (K)

Departments of Neurology and Ophthalmology, University of Kentucky, Lexington, 40506, USA.

Charles K Abrams (CK)

Department of Neurology and Rehabilitation, College of Medicine, University of Illinois at Chicago, Chicago, IL, 60607, USA.

Pasquale Striano (P)

Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genoa, 16132, Genoa, Italy.
Pediatric Neurology and Muscular Diseases Unit, IRCCS Giannina Gaslini Institute, 16147, Genoa, Italy.

Sara Fortuna (S)

Computational Modelling of Nanoscale and Biophysical Systems Laboratory, Italian Institute of Technology, 16163, Genoa, Italy.
Department of Chemical and Pharmaceutical Sciences, University of Trieste, 34134, Trieste, Italy.

Reza Maroofian (R)

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

Henry Houlden (H)

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

Federico Zara (F)

Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genoa, 16132, Genoa, Italy.
Unit of Medical Genetics, IRCCS Istituto Giannina Gaslini, 16147, Genoa, Italy.

Chiara Fiorillo (C)

Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genoa, 16132, Genoa, Italy. chiarafiorillo@gaslini.org.
Pediatric Neurology and Muscular Diseases Unit, IRCCS Giannina Gaslini Institute, 16147, Genoa, Italy. chiarafiorillo@gaslini.org.

Vincenzo Salpietro (V)

Department of Neuromuscular Disorders, Queen Square Institute of Neurology, University College London, London, WC1N 3BG, UK. v.salpietro@ucl.ac.uk.
Department of Biotechnological and Applied Clinical Sciences, University of L'Aquila, 67100, L'Aquila, Italy. v.salpietro@ucl.ac.uk.

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