A deep intronic splice–altering AIRE variant causes APECED syndrome through antisense oligonucleotide-targetable pseudoexon inclusion

Глубокий интронный вариант AIRE, нарушающий сплайсинг, вызывает синдром APECED посредством включения псдоэкзона, на которое можно воздействовать антисмысловым олигонуклеотидом
Sebastian Ochoa, Amy P. Hsu, Andrew J. Oler, Dhaneshwar Kumar, Daniel Chauss, Jan Piet van Hamburg, Gustaaf G. van Laar, Vasileios Oikonomou, Sundar Ganesan, Elise M. N. Ferré, Monica M. Schmitt, Tom DiMaggio, Princess Barber, Gregory Constantine, Lindsey B. Rosen, Paul G. Auwaerter, Bhumika Gandhi, Jennifer L. Miller, Rachel Eisenberg, Arye Rubinstein, Edith Schussler, Erjola Balliu, Vandana Shashi, Olaf Neth, Peter Olbrich, Kim My Le, Nanni Mamia, Saila Laakso, Pasi I. Nevalainen, Juha Grönholm, Mikko Seppänen, Louis Boon, Gulbu Uzel, Luis M. Franco, Theo Heller, Karen K. Winer, Rajarshi Ghosh, Bryce A. Seifert, Magdalena Walkiewicz, Luigi D. Notarangelo, Qing Zhou, Ivona Askentijevich, William A. Gahl, Cliffton L. Dalgard, L. Perera, Behdad Afzali, Sander W. Tas, Steven M. Holland, Michail S. Lionakis
2024-09-18

AIRE variantAPECED syndromeantisense oligonucleotidedeep intronic variantpseudoexon inclusion
Autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED) is a life-threatening monogenic autoimmune disorder primarily caused by biallelic deleterious variants in the autoimmune regulator ( AIRE ) gene. We prospectively evaluated 104 patients with clinically diagnosed APECED syndrome and identified 17 patients (16%) from 14 kindreds lacking biallelic AIRE variants in exons or flanking intronic regions; 15 had Puerto Rican ancestry. Through whole-genome sequencing, we identified a deep intronic AIRE variant (c.1504-818 G>A) cosegregating with the disease in all 17 patients. We developed a culture system of AIRE -expressing primary patient monocyte-derived dendric cells and demonstrated that c.1504-818 G>A creates a cryptic splice site and activates inclusion of a 109–base pair frame-shifting pseudoexon. We also found low-level AIRE expression in patient-derived lymphoblastoid cell lines (LCLs) and confirmed pseudoexon inclusion in independent extrathymic AIRE –expressing cell lines. Through protein modeling and transcriptomic analyses of AIRE -transfected human embryonic kidney 293 and thymic epithelial cell 4D6 cells, we showed that this variant alters the carboxyl terminus of the AIRE protein, abrogating its function. Last, we developed an antisense oligonucleotide (ASO) that reversed pseudoexon inclusion and restored the normal AIRE transcript sequence in LCLs. Thus, our findings revealed c.1504-818 G>A as a founder APECED-causing AIRE variant in the Puerto Rican population and uncovered pseudoexon inclusion as an ASO-reversible genetic mechanism underlying APECED.
1
Among 104 clinically diagnosed APECED patients, 17 individuals from 14 kindreds lacked coding or canonical splice-region AIRE variants; 15 had Puerto Rican ancestry.
2
An antisense oligonucleotide reversed pseudoexon inclusion and restored the normal AIRE transcript sequence in patient-derived lymphoblastoid cell lines, demonstrating therapeutic reversibility.
3
Pseudoexon inclusion alters the AIRE protein’s carboxyl terminus and abolishes its function, establishing the molecular mechanism causing APECED.
4
The variant creates a cryptic splice site that causes inclusion of a 109-base-pair frameshifting pseudoexon in AIRE transcripts.
5
Whole-genome sequencing identified the deep intronic AIRE variant c.1504-818 G>A, which cosegregated with APECED in all 17 patients and represents a Puerto Rican founder variant.

the deep intronic AIRE variant c.1504-818 G>A and its effects on AIRE expression in APECED patient-derived cells

cryptic splice-site activation, 109-bp frameshifting pseudoexon inclusion, resultant AIRE dysfunction, and antisense-oligonucleotide-mediated correction

Publication Details
Publication Date
2024-09-18
Journal
Publisher
ISSN
Cited by
16
Access Type
Author Information
Authors
Sebastian Ochoa
Amy P. Hsu
Andrew J. Oler
Dhaneshwar Kumar
Daniel Chauss
Jan Piet van Hamburg
Gustaaf G. van Laar
Vasileios Oikonomou
Sundar Ganesan
Elise M. N. Ferré
Monica M. Schmitt
Tom DiMaggio
Princess Barber
Gregory Constantine
Lindsey B. Rosen
Paul G. Auwaerter
Bhumika Gandhi
Jennifer L. Miller
Rachel Eisenberg
Arye Rubinstein
Edith Schussler
Erjola Balliu
Vandana Shashi
Olaf Neth
Peter Olbrich
Kim My Le
Nanni Mamia
Saila Laakso
Pasi I. Nevalainen
Juha Grönholm
Mikko Seppänen
Louis Boon
Gulbu Uzel
Luis M. Franco
Theo Heller
Karen K. Winer
Rajarshi Ghosh
Bryce A. Seifert
Magdalena Walkiewicz
Luigi D. Notarangelo
Qing Zhou
Ivona Askentijevich
William A. Gahl
Cliffton L. Dalgard
L. Perera
Behdad Afzali
Sander W. Tas
Steven M. Holland
Michail S. Lionakis
Explore further
Open the scid.ai AI chat with a ready-made request: it will find papers on a similar topic and help build a literature review.
Find similar papers in the chat
Make a presentation
100%