Next generation sequencing analysis reveals complex genetic architecture of childhood-onset systemic lupus erythematosus

Objectives Our current understanding of the genetic architecture of childhood-onset SLE (cSLE) is limited by a dearth of comprehensive genomic studies in cSLE. We have quantified the number of known rare and common SLE risk variants in a diverse cSLE cohort. We characterised type I interferon (IFN)...

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Main Authors: Mariana J Kaplan, Sarfaraz Hasni, Ivona Aksentijevich, Earl D Silverman, Shajia Lu, Massimo Gadina, Michael J Ombrello, Diana Gómez-Martín, Christiaan Scott, Ana Barrera-Vargas, Zuoming Deng, Laura Lewandowski, Linda Hiraki, Jorge Romo Tena, Anthony M Musolf, Subrata Paul, Daniel Hupalo, Clifton L Dalgard
Format: Article
Language:English
Published: BMJ Publishing Group 2025-06-01
Series:Lupus Science and Medicine
Online Access:https://lupus.bmj.com/content/12/1/e001475.full
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author Mariana J Kaplan
Sarfaraz Hasni
Ivona Aksentijevich
Earl D Silverman
Shajia Lu
Massimo Gadina
Michael J Ombrello
Diana Gómez-Martín
Christiaan Scott
Ana Barrera-Vargas
Zuoming Deng
Laura Lewandowski
Linda Hiraki
Jorge Romo Tena
Anthony M Musolf
Subrata Paul
Daniel Hupalo
Clifton L Dalgard
author_facet Mariana J Kaplan
Sarfaraz Hasni
Ivona Aksentijevich
Earl D Silverman
Shajia Lu
Massimo Gadina
Michael J Ombrello
Diana Gómez-Martín
Christiaan Scott
Ana Barrera-Vargas
Zuoming Deng
Laura Lewandowski
Linda Hiraki
Jorge Romo Tena
Anthony M Musolf
Subrata Paul
Daniel Hupalo
Clifton L Dalgard
author_sort Mariana J Kaplan
collection DOAJ
description Objectives Our current understanding of the genetic architecture of childhood-onset SLE (cSLE) is limited by a dearth of comprehensive genomic studies in cSLE. We have quantified the number of known rare and common SLE risk variants in a diverse cSLE cohort. We characterised type I interferon (IFN) gene expression scores along with genomic data.Methods We performed whole genome sequencing on 83 patients with cSLE and 109 unaffected parents and analysed sequences for known common and rare SLE-associated risk variants. Type I IFN gene expression was quantified on a subset of patients. We investigated the relationship between clinical phenotype, genomic profile and type I IFN signatures in this cohort.Results Patients with cSLE were enriched for common SLE risk variants compared with unaffected parents and controls. We identified rare SLE risk variants in 11% of individuals with cSLE; those with rare variants had earlier disease onset (<12 years) than those without variants. Patients with cSLE had elevated type I IFN gene expression compared with unaffected parents and controls, even though most patients were treated with immunosuppressive therapy.Conclusions Patients with cSLE from this ancestrally and geographically diverse cohort are enriched for common cSLE risk variants compared with controls, and 11% carry a rare variant in known monogenic SLE risk genes. The relationship between rare and common risk variant burden is more complex than previously hypothesised. Our findings indicate that studying patients with cSLE is important for understanding genetic contributions to SLE pathogenesis.
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spelling doaj-art-a53aad8361ed4e7b8aafe8939ec8215a2025-08-20T02:33:11ZengBMJ Publishing GroupLupus Science and Medicine2053-87902025-06-0112110.1136/lupus-2024-001475Next generation sequencing analysis reveals complex genetic architecture of childhood-onset systemic lupus erythematosusMariana J Kaplan0Sarfaraz Hasni1Ivona Aksentijevich2Earl D Silverman3Shajia Lu4Massimo Gadina5Michael J Ombrello6Diana Gómez-Martín7Christiaan Scott8Ana Barrera-Vargas9Zuoming Deng10Laura Lewandowski11Linda Hiraki12Jorge Romo Tena13Anthony M Musolf14Subrata Paul15Daniel Hupalo16Clifton L Dalgard17Systemic Autoimmunity Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USALupus Clinical Research, Office of the Clinical Director, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USAInflammatory Disease Section, National Human Genome Research Institute, Bethesda, Maryland, USARheumatology, The Hospital for Sick Children, Toronto, Ontario, CanadaTranslational Immunology Section, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USATranslational Immunology Section, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USATranslational Genetics and Genomics Unit, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USAImmunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, MexicoDepartment of Paediatrics and Child Health, Red Cross War Memorial Children’s Hospital and University of Cape Town, Cape Town, South AfricaImmunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, MexicoBiodata Mining and Discovery Section, Office of Science and Technology, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USAIntramural Research Program, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USARheumatology, The Hospital for Sick Children, Toronto, Ontario, CanadaImmunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, MexicoComputational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland, USACollaborative Bioinformatics Resource, NIAID, Bethesda, Maryland, USAThe American Genome Center, Department of Anatomy, Physiology & Genetics, Uniformed Services University, Bethesda, Maryland, USAThe American Genome Center, Department of Anatomy, Physiology & Genetics, Uniformed Services University, Bethesda, Maryland, USAObjectives Our current understanding of the genetic architecture of childhood-onset SLE (cSLE) is limited by a dearth of comprehensive genomic studies in cSLE. We have quantified the number of known rare and common SLE risk variants in a diverse cSLE cohort. We characterised type I interferon (IFN) gene expression scores along with genomic data.Methods We performed whole genome sequencing on 83 patients with cSLE and 109 unaffected parents and analysed sequences for known common and rare SLE-associated risk variants. Type I IFN gene expression was quantified on a subset of patients. We investigated the relationship between clinical phenotype, genomic profile and type I IFN signatures in this cohort.Results Patients with cSLE were enriched for common SLE risk variants compared with unaffected parents and controls. We identified rare SLE risk variants in 11% of individuals with cSLE; those with rare variants had earlier disease onset (<12 years) than those without variants. Patients with cSLE had elevated type I IFN gene expression compared with unaffected parents and controls, even though most patients were treated with immunosuppressive therapy.Conclusions Patients with cSLE from this ancestrally and geographically diverse cohort are enriched for common cSLE risk variants compared with controls, and 11% carry a rare variant in known monogenic SLE risk genes. The relationship between rare and common risk variant burden is more complex than previously hypothesised. Our findings indicate that studying patients with cSLE is important for understanding genetic contributions to SLE pathogenesis.https://lupus.bmj.com/content/12/1/e001475.full
spellingShingle Mariana J Kaplan
Sarfaraz Hasni
Ivona Aksentijevich
Earl D Silverman
Shajia Lu
Massimo Gadina
Michael J Ombrello
Diana Gómez-Martín
Christiaan Scott
Ana Barrera-Vargas
Zuoming Deng
Laura Lewandowski
Linda Hiraki
Jorge Romo Tena
Anthony M Musolf
Subrata Paul
Daniel Hupalo
Clifton L Dalgard
Next generation sequencing analysis reveals complex genetic architecture of childhood-onset systemic lupus erythematosus
Lupus Science and Medicine
title Next generation sequencing analysis reveals complex genetic architecture of childhood-onset systemic lupus erythematosus
title_full Next generation sequencing analysis reveals complex genetic architecture of childhood-onset systemic lupus erythematosus
title_fullStr Next generation sequencing analysis reveals complex genetic architecture of childhood-onset systemic lupus erythematosus
title_full_unstemmed Next generation sequencing analysis reveals complex genetic architecture of childhood-onset systemic lupus erythematosus
title_short Next generation sequencing analysis reveals complex genetic architecture of childhood-onset systemic lupus erythematosus
title_sort next generation sequencing analysis reveals complex genetic architecture of childhood onset systemic lupus erythematosus
url https://lupus.bmj.com/content/12/1/e001475.full
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