Unproductive alternative splicing of ATM exon 7: mapping of critical regulatory elements and identification of 34 spliceogenic variants

ATM loss-of-function variants are significantly associated with increased breast cancer risk. ATM exon 7 skipping (△(E7)) is a naturally-occurring alternative splicing event, which introduces a premature termination codon and represents a form of gene-expression regulation via unproductive splicing....

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Detalles Bibliográficos
Autores: Llinares-Burguet, Inés, Sanoguera-Miralles, Lara, García-Álvarez, Alicia, Esteban-Sánchez, Ada, Caloca, María J., Hoya, Miguel de la, Bueno-Martínez, Elena, Velasco, Eladio
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2025
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/400631
Acceso en línea:http://hdl.handle.net/10261/400631
Access Level:acceso abierto
Palabra clave:Hereditary breast cancer
ATM
Variants of uncertain significance
Unproductive splicing
Aberrant splicing
Splicing regulatory elements
Minigenes
Descripción
Sumario:ATM loss-of-function variants are significantly associated with increased breast cancer risk. ATM exon 7 skipping (△(E7)) is a naturally-occurring alternative splicing event, which introduces a premature termination codon and represents a form of gene-expression regulation via unproductive splicing. Disruption of splicing regulatory elements (SRE) by variants can lead to mis-splicing, potentially contributing to disease susceptibility. To study the regulatory mechanisms of △(E7) and the impact of exonic variants on splicing, a combined in silico/minigene approach was employed, using the construct mgATM_4-9 (exons 4–9) that recapitulates this splicing event. HEXplorer analysis of ATM exon 7 predicted two splicing enhancer-rich regions (c.665–681 and c.867–898). Deletions of these intervals in mgATM_4-9 significantly increased △(E7) (57–96%), revealing their critical role for exon 7 inclusion. Forty-eight candidate variants (HEXplorer, △HZEI score < -40) within these SRE-rich segments were functionally assayed, 34 of which (71%) impaired exon 7 recognition. Nineteen variants presented strong impacts with high expression of △(E7)-transcripts (69–96%), of which c.668A > T, c.680C > A and c.680C > T exhibited particularly strong effects (4–13% full-length transcripts). DeepCLIP analysis suggested that SR proteins SRSF7 and SRSF10 play a positive regulatory role in exon 7 inclusion. Eight variants were classified as likely pathogenic according to ACMG/AMP-based guidelines. Furthermore, nine missense and two synonymous variants with strong impacts (16–29% full-length transcripts) might represent intermediate risk alleles. This work collectively demonstrates the intricate nature of ATM exon 7 recognition, regulated by cis-acting SREs, emphasizing the value of in silico predictions for initial variant filtering and minigene assays for dissecting splicing regulation and clinical interpretation of variants.