Faculty, Staff and Student Publications

Language

English

Publication Date

8-19-2025

Journal

Circulation

DOI

10.1161/CIRCULATIONAHA.125.074218

PMID

40378078

PMCID

PMC12220935

PubMedCentral® Posted Date

5-16-2025

PubMedCentral® Full Text Version

Post-print

Abstract

Background: Vascular smooth muscle cells (SMCs), the predominant cell type in the aortic wall, play a crucial role in maintaining aortic integrity, blood pressure, and cardiovascular function. Vascular SMC contractility and function depend on ACTA2 (smooth muscle α-actin 2). The pathogenic variant ACTA2 c.536G>A (p.R179H) causes multisystemic smooth muscle dysfunction syndrome, a severe disorder marked by widespread smooth muscle abnormalities, resulting in life-threatening aortic disease and high risk of early death from aneurysms or stroke. No effective treatments exist for multisystemic smooth muscle dysfunction syndrome.

Methods: To develop a comprehensive therapy for multisystemic smooth muscle dysfunction syndrome, we used CRISPR (clustered regularly interspaced short palindromic repeats)-Cas9 (CRISPR-associated protein 9) adenine base editing to correct the ACTA2 R179H sequence variant. We generated isogenic human induced pluripotent stem cell lines and humanized mice carrying this pathogenic missense sequence variant. Induced pluripotent stem cell-derived SMCs were evaluated for key functional characteristics, including proliferation, migration, and contractility. The adenine base editor ABE8e-SpCas9-VRQR under control of either an SMC-specific promoter or a cytomegalovirus promoter, and an optimized single guide RNA under control of a U6 promoter were delivered intravenously to humanized R179H mice using adeno-associated virus serotype 9 and phenotypic outcomes were evaluated.

Results: The R179H sequence variant causes a dramatic phenotypic switch in human induced pluripotent stem cell-derived SMCs from a contractile to a synthetic state, a transition associated with aneurysm formation. Base editing prevented this pathogenic phenotypic switch and restored normal SMC function. In humanized mice, the ACTA2R179H/+ sequence variant caused widespread smooth muscle dysfunction, manifesting as decreased blood pressure, aortic dilation and dissection, bladder enlargement, gut dilation, and hydronephrosis. In vivo base editing rescued these pathological abnormalities, normalizing smooth muscle function.

Conclusions: This study demonstrates the effectiveness of adenine base editing to treat multisystemic smooth muscle dysfunction syndrome and restore aortic smooth muscle function. By correcting the ACTA2 R179H sequence variant, the pathogenic phenotypic shift in SMCs was prevented, key aortic smooth muscle functions were restored, and life-threatening aortic dilation and dissection were mitigated in humanized mice. These findings underscore the promise of gene-editing therapies in addressing the underlying genetic causes of smooth muscle disorders and offer a potential transformative treatment for patients facing severe vascular complications.

Keywords

Animals, Gene Editing, Humans, Mice, Actins, Muscle, Smooth, Vascular, Myocytes, Smooth Muscle, Induced Pluripotent Stem Cells, CRISPR-Cas Systems, Disease Models, Animal, Genetic Therapy, aortic aneurysm; gene editing; muscle, smooth

Published Open-Access

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