HPDL Variant Type Correlates With Clinical Disease Onset and Severity

ABSTRACT Objective Recently, a mitochondrial encephalopathy due to biallelic HPDL variants was described, associated with a broad range of clinical manifestations ranging from severe, infantile‐onset neurodegeneration to adolescence‐onset hereditary spastic paraplegia. HPDL converts 4‐hydroxyphenylp...

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Main Authors: Eun Hye Lee, Olivia Kim‐Mcmanus, Jennifer H. Yang, Richard Haas, Maha S. Zaki, Ghada M. H. Abdel‐Salam, Yuji Nakamura, Mohamed S. Abdel‐Hamind, Darius Ebrahimi‐Fakhari, Julian E. Alecu, Nicola Brunetti‐Pierri, Varunvenkat M. Srinivasan, Vykuntaraju K. Gowda, Stephanie Gross, Yasemin Alanay, Paria Najarzadeh Totbati, Manya Yadavilli, Liana Friedman, Naomi Meave Ojeda, Joseph G. Gleeson
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:Annals of Clinical and Translational Neurology
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Online Access:https://doi.org/10.1002/acn3.70047
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author Eun Hye Lee
Olivia Kim‐Mcmanus
Jennifer H. Yang
Richard Haas
Maha S. Zaki
Ghada M. H. Abdel‐Salam
Yuji Nakamura
Mohamed S. Abdel‐Hamind
Darius Ebrahimi‐Fakhari
Julian E. Alecu
Nicola Brunetti‐Pierri
Varunvenkat M. Srinivasan
Vykuntaraju K. Gowda
Stephanie Gross
Yasemin Alanay
Paria Najarzadeh Totbati
Manya Yadavilli
Liana Friedman
Naomi Meave Ojeda
Joseph G. Gleeson
author_facet Eun Hye Lee
Olivia Kim‐Mcmanus
Jennifer H. Yang
Richard Haas
Maha S. Zaki
Ghada M. H. Abdel‐Salam
Yuji Nakamura
Mohamed S. Abdel‐Hamind
Darius Ebrahimi‐Fakhari
Julian E. Alecu
Nicola Brunetti‐Pierri
Varunvenkat M. Srinivasan
Vykuntaraju K. Gowda
Stephanie Gross
Yasemin Alanay
Paria Najarzadeh Totbati
Manya Yadavilli
Liana Friedman
Naomi Meave Ojeda
Joseph G. Gleeson
author_sort Eun Hye Lee
collection DOAJ
description ABSTRACT Objective Recently, a mitochondrial encephalopathy due to biallelic HPDL variants was described, associated with a broad range of clinical manifestations ranging from severe, infantile‐onset neurodegeneration to adolescence‐onset hereditary spastic paraplegia. HPDL converts 4‐hydroxyphenylpyruvate acid (4‐HPPA) into 4‐hydroxymandelate (4‐HMA), necessary for the synthesis of the mitochondrial electron transporter CoQ10. This suggests a possible bypass of the metabolic block by 4‐HMA treatment; however, genotype–phenotype correlations are lacking. Methods We established an HPDL Patient Registry to prepare for a future clinical trial. Here we report the clinical features of 13 enrolled participants and compare them with 86 previously reported patients. We establish three major clinical classes: severe, intermediate, and mild, presenting onset in early infancy, childhood, and adolescence, respectively. The biallelic genotypes were classified into truncating/truncating, truncating/missense, and missense/missense variants, mapped onto the predicted 3D protein structure, and correlated with severity. Results Patients with biallelic truncating variants presented with severe phenotypes and earlier ages of onset. Missense variants were often associated with milder phenotypes, except those with variants predominantly located in or near the VOC2 domain containing iron‐binding sites or the C‐terminus, which had more severe phenotypes. In addition, p.Met1? variants were also correlated with more severe phenotypes. Interpretation This study demonstrates the correlation of age of onset and disease severity with genotype for HPDL‐related conditions. Patients with truncating variants and specific missense variants correlated with severe, early‐onset features, whereas the presence of at least one missense variant located outside of the iron‐binding sites correlated with milder presentations. Trial Registration Clinicaltrials.gov HPDL registry: https://clinicaltrials.gov/study/NCT05848271
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spelling doaj-art-34d4f1ef2261415182bf82888f65d3f22025-08-20T03:27:19ZengWileyAnnals of Clinical and Translational Neurology2328-95032025-07-011271360136710.1002/acn3.70047HPDL Variant Type Correlates With Clinical Disease Onset and SeverityEun Hye Lee0Olivia Kim‐Mcmanus1Jennifer H. Yang2Richard Haas3Maha S. Zaki4Ghada M. H. Abdel‐Salam5Yuji Nakamura6Mohamed S. Abdel‐Hamind7Darius Ebrahimi‐Fakhari8Julian E. Alecu9Nicola Brunetti‐Pierri10Varunvenkat M. Srinivasan11Vykuntaraju K. Gowda12Stephanie Gross13Yasemin Alanay14Paria Najarzadeh Totbati15Manya Yadavilli16Liana Friedman17Naomi Meave Ojeda18Joseph G. Gleeson19Rady Children's Institute for Genomic Medicine San Diego California USADepartment of Neurosciences and Pediatrics University of California San Diego California USADepartment of Neurosciences and Pediatrics University of California San Diego California USADepartment of Neurosciences and Pediatrics University of California San Diego California USAHuman Genetics and Genome Research Division, Clinical Genetics Department National Research Centre Cairo EgyptHuman Genetics and Genome Research Division, Clinical Genetics Department National Research Centre Cairo EgyptRady Children's Institute for Genomic Medicine San Diego California USAHuman Genetics and Genome Research Division, Medical Molecular Genetic Department National Research Centre Cairo EgyptDepartment of Neurology, F.M. Kirby Neurobiology Center, Boston Children's Hospital Harvard Medical School Boston Massachusetts USADepartment of Neurology, F.M. Kirby Neurobiology Center, Boston Children's Hospital Harvard Medical School Boston Massachusetts USATelethon Institute of Genetics and Medicine Naples ItalyDepartment of Pediatric Neurology Indira Gandhi Institute of Child Health Bangalore IndiaDepartment of Pediatric Neurology Indira Gandhi Institute of Child Health Bangalore IndiaDepartment of Pediatric Neurology, Social Pediatrics and Epileptology Center for Pediatrics and Adolescent Medicine at the University Hospital Giessen and Marburg GmbH Marburg GermanyPediatric Genetics Unit, Department of Pediatrics, School of Medicine Acibadem Mehmet Ali Aydinlar University Istanbul TurkeyPediatric Genetics Unit, Department of Pediatrics, School of Medicine Acibadem Mehmet Ali Aydinlar University Istanbul TurkeyRady Children's Institute for Genomic Medicine San Diego California USARady Children's Institute for Genomic Medicine San Diego California USARady Children's Institute for Genomic Medicine San Diego California USARady Children's Institute for Genomic Medicine San Diego California USAABSTRACT Objective Recently, a mitochondrial encephalopathy due to biallelic HPDL variants was described, associated with a broad range of clinical manifestations ranging from severe, infantile‐onset neurodegeneration to adolescence‐onset hereditary spastic paraplegia. HPDL converts 4‐hydroxyphenylpyruvate acid (4‐HPPA) into 4‐hydroxymandelate (4‐HMA), necessary for the synthesis of the mitochondrial electron transporter CoQ10. This suggests a possible bypass of the metabolic block by 4‐HMA treatment; however, genotype–phenotype correlations are lacking. Methods We established an HPDL Patient Registry to prepare for a future clinical trial. Here we report the clinical features of 13 enrolled participants and compare them with 86 previously reported patients. We establish three major clinical classes: severe, intermediate, and mild, presenting onset in early infancy, childhood, and adolescence, respectively. The biallelic genotypes were classified into truncating/truncating, truncating/missense, and missense/missense variants, mapped onto the predicted 3D protein structure, and correlated with severity. Results Patients with biallelic truncating variants presented with severe phenotypes and earlier ages of onset. Missense variants were often associated with milder phenotypes, except those with variants predominantly located in or near the VOC2 domain containing iron‐binding sites or the C‐terminus, which had more severe phenotypes. In addition, p.Met1? variants were also correlated with more severe phenotypes. Interpretation This study demonstrates the correlation of age of onset and disease severity with genotype for HPDL‐related conditions. Patients with truncating variants and specific missense variants correlated with severe, early‐onset features, whereas the presence of at least one missense variant located outside of the iron‐binding sites correlated with milder presentations. Trial Registration Clinicaltrials.gov HPDL registry: https://clinicaltrials.gov/study/NCT05848271https://doi.org/10.1002/acn3.700474‐hydroxyphenylpyruvate dioxygenase‐like proteinencephalopathyhereditary spastic paraplegiaHPDLmitochondria
spellingShingle Eun Hye Lee
Olivia Kim‐Mcmanus
Jennifer H. Yang
Richard Haas
Maha S. Zaki
Ghada M. H. Abdel‐Salam
Yuji Nakamura
Mohamed S. Abdel‐Hamind
Darius Ebrahimi‐Fakhari
Julian E. Alecu
Nicola Brunetti‐Pierri
Varunvenkat M. Srinivasan
Vykuntaraju K. Gowda
Stephanie Gross
Yasemin Alanay
Paria Najarzadeh Totbati
Manya Yadavilli
Liana Friedman
Naomi Meave Ojeda
Joseph G. Gleeson
HPDL Variant Type Correlates With Clinical Disease Onset and Severity
Annals of Clinical and Translational Neurology
4‐hydroxyphenylpyruvate dioxygenase‐like protein
encephalopathy
hereditary spastic paraplegia
HPDL
mitochondria
title HPDL Variant Type Correlates With Clinical Disease Onset and Severity
title_full HPDL Variant Type Correlates With Clinical Disease Onset and Severity
title_fullStr HPDL Variant Type Correlates With Clinical Disease Onset and Severity
title_full_unstemmed HPDL Variant Type Correlates With Clinical Disease Onset and Severity
title_short HPDL Variant Type Correlates With Clinical Disease Onset and Severity
title_sort hpdl variant type correlates with clinical disease onset and severity
topic 4‐hydroxyphenylpyruvate dioxygenase‐like protein
encephalopathy
hereditary spastic paraplegia
HPDL
mitochondria
url https://doi.org/10.1002/acn3.70047
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