Authors

Ivana Lessel
Anja Baresic
Ivan K Chinn
Jonathan May
Anu Goenka
Kate E Chandler
Jennifer E Posey
Alexandra Afenjar
Luisa Averdunk
Maria Francesca Bedeschi
Thomas Besnard
Rae Brager
Lauren Brick
Melanie Brugger
Theresa Brunet
Susan Byrne
Oscar de la Calle-Martín
Valeria Capra
Paul Cardenas
Céline Chappé
Hey J Chong
Benjamin Cogne
Erin Conboy
Heidi Cope
Thomas Courtin
Wallid Deb
Robertino Dilena
Christèle Dubourg
Magdeldin Elgizouli
Erica Fernandes
Kristi K Fitzgerald
Silvana Gangi
Jaya K George-Abraham
Muge Gucsavas-Calikoglu
Tobias B Haack
Medard Hadonou
Britta Hanker
Irina Hüning
Maria Iascone
Bertrand Isidor
Irma Järvelä
Jay J Jin
Alexander A L Jorge
Dragana Josifova
Ruta Kalinauskiene
Erik-Jan Kamsteeg
Boris Keren
Elena Kessler
Heike Kölbel
Mariya Kozenko
Christian Kubisch
Alma Kuechler
Suzanne M Leal
Juha Leppälä
Sharon M Luu
Gholson J Lyon
Suneeta Madan-Khetarpal
Margherita Mancardi
Elaine Marchi
Lakshmi Mehta
Beatriz Menendez
Chantal F Morel
Sue Moyer Harasink
Dayna-Lynn Nevay
Vincenzo Nigro
Sylvie Odent
Renske Oegema
John Pappas
Matthew T Pastore
Yezmin Perilla-Young
Konrad Platzer
Nina Powell-Hamilton
Rachel Rabin
Aisha Rekab
Raissa C Rezende
Leema Robert
Ferruccio Romano
Marcello Scala
Karin Poths
Isabelle Schrauwen
Jessica Sebastian
John Short
Richard Sidlow
Jennifer Sullivan
Katalin Szakszon
Queenie K G Tan
Undiagnosed Diseases Network
Matias Wagner
Dagmar Wieczorek
Bo Yuan
Nicole Maeding
Dirk Strunk
Amber Begtrup
Siddharth Banka
James R Lupski
Eva Tolosa
Davor Lessel

Publication Date

2-6-2025

Journal

American Journal of Human Genetics

DOI

10.1016/j.ajhg.2024.12.012

PMID

39798569

PMCID

PMC11866971

PubMedCentral® Posted Date

1-10-2025

PubMedCentral® Full Text Version

Post-print

Abstract

BCL11B is a Cys2-His2 zinc-finger (C2H2-ZnF) domain-containing, DNA-binding, transcription factor with established roles in the development of various organs and tissues, primarily the immune and nervous systems. BCL11B germline variants have been associated with a variety of developmental syndromes. However, genotype-phenotype correlations along with pathophysiologic mechanisms of selected variants mostly remain elusive. To dissect these, we performed genotype-phenotype correlations of 92 affected individuals harboring a pathogenic or likely pathogenic BCL11B variant, followed by immune phenotyping, analysis of chromatin immunoprecipitation DNA-sequencing data, dual-luciferase reporter assays, and molecular modeling. These integrative analyses enabled us to define three clinical subtypes of BCL11B-related disorders. It is likely that gene-disruptive BCL11B variants and missense variants affecting zinc-binding cysteine and histidine residues cause mild to moderate neurodevelopmental delay with increased propensity for behavioral and dental anomalies, allergies and asthma, and reduced type 2 innate lymphoid cells. Missense variants within C2H2-ZnF DNA-contacting α helices cause highly variable clinical presentations ranging from multisystem anomalies with demise in the first years of life to late-onset, hyperkinetic movement disorder with poor fine motor skills. Those not in direct DNA contact cause a milder phenotype through reduced, target-specific transcriptional activity. However, missense variants affecting C2H2-ZnFs, DNA binding, and "specificity residues" impair BCL11B transcriptional activity in a target-specific, dominant-negative manner along with aberrant regulation of alternative DNA targets, resulting in more severe and unpredictable clinical outcomes. Taken together, we suggest that the phenotypic severity and variability is largely dependent on the DNA-binding affinity and specificity of altered BCL11B proteins.

Keywords

Adolescent, Child, Child, Preschool, Female, Infant, Male, Young Adult, Amino Acid Sequence, Binding Sites, Developmental Disabilities, DNA-Binding Proteins, Genome, Human, HEK293 Cells, Mutation, Phenotype, Protein Binding, Tumor Suppressor Proteins, Zinc Fingers, Humans, BCL11B, C2H2-type zinc finger protein, recognition code, genotype-phenotype correlation, type 2 innate lymphoid cells

Published Open-Access

yes

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