Genes that escape X chromosome inactivation modulate sex differences in valve myofibroblasts
Open accessAbstract
Background: Aortic valve stenosis is a sexually dimorphic disease, with women often presenting with sustained fibrosis and men with more extensive calcification. However, the intracellular molecular mechanisms that drive these clinically important sex differences remain underexplored. Methods: Hydrogel biomaterials were designed to recapitulate key aspects of the valve tissue microenvironment and to serve as a culture platform for sex-specific valvular interstitial cells (VICs; precursors to profibrotic myofibroblasts). The hydrogel culture system was used to interrogate intracellular pathways involved in sex-dependent VIC-to-myofibroblast activation and deactivation. RNA sequencing was used to define pathways involved in driving sex-dependent activation. Interventions with small molecule inhibitors and siRNA transfections were performed to provide mechanistic insight into sex-specific cellular responses to microenvironmental cues, including matrix stiffness and exogenously delivered biochemical factors. Results: In both healthy porcine and human aortic valves, female leaflets had higher baseline activation of the myofibroblast marker α-smooth muscle actin compared with male leaflets. When isolated and cultured, female porcine and human VICs had higher levels of basal α-smooth muscle actin stress fibers that further increased in response to the hydrogel matrix stiffness, both of which were higher than in male VICs. A transcriptomic analysis of male and female porcine VICs revealed Rho-associated protein kinase signaling as a potential driver of this sex-dependent myofibroblast activation. Furthermore, we found that genes that escape X-chromosome inactivation such as BMX and STS (encoding for Bmx nonreceptor tyrosine kinase and steroid sulfatase, respectively) partially regulate the elevated female myofibroblast activation through Rho-associated protein kinase signaling. This finding was confirmed by treating male and female VICs with endothelin-1 and plasminogen activator inhibitor-1, factors that are secreted by endothelial cells and known to drive myofibroblast activation through Rho-associated protein kinase signaling. Conclusions: Together, in vivo and in vitro results confirm sex dependencies in myofibroblast activation pathways and implicate genes that escape X-chromosome inactivation in regulating sex differences in myofibroblast activation and subsequent aortic valve stenosis progression. Our results underscore the importance of considering sex as a biological variable to understand the molecular mechanisms of aortic valve stenosis and to help guide sex-based precision therapies.
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Recent work with porcine aortic valves suggested that genes escaping X-chromosome inactivation may contribute to the progression of calcific aortic valve stenosis.
“Recent work with porcine aortic valves suggested that genes escaping X-chromosome inactivation (XCI) may contribute to the progression of CAVS 12 .”
From Sex-specific gene expression signatures of calcific aortic valve stenosis in a large collection of human tissues (2026) · cites this paper as [12]
Sex chromosomes represent a plausible origin for the sexual dimorphism observed consistently in CAVS at the cellular and tissue levels.
“Sex chromosomes represent a plausible origin for the sexual dimorphism that has been observed consistently in CAVS at the cellular and tissue levels 9,12,52 .”
From Sex-specific gene expression signatures of calcific aortic valve stenosis in a large collection of human tissues (2026) · cites this paper as [12]
In a previous study, PRKX was significantly upregulated in myofibroblasts compared to fibroblasts in both female and male porcine valve interstitial cells.
“In a previous study, it was significantly upregulated in myofibroblasts compared to fibroblasts in both female and male porcine valve interstitial cells 12 .”
From Sex-specific gene expression signatures of calcific aortic valve stenosis in a large collection of human tissues (2026) · cites this paper as [12]
The Results section reports differential gene expression between fibroblast-like and myofibroblast-like porcine valve interstitial cells, but the passages retrieved by searching for PRKX do not mention that gene. Our copy therefore does not establish whether PRKX was significantly upregulated in both female and male cells. (LLM, conf=0.72)
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- Authors
- Aguado, B. A., Walker, C. J., Grim, J. C., Schroeder, M. E., Batan, D., Vogt, B. J., Rodriguez, A. G., Schwisow, J. A., Moulton, K. S., Weiss, R. M., Heistad, D. D., Leinwand, L. A., & Anseth, K. S.
- Affiliations
- University of Colorado Boulder (US)
- University of Colorado Anschutz (US)
- University of Iowa (US)
- Corresponding author
- Leinwand, Leslie A.
- Anseth, Kristi S.
- ORCID
- Venue
- Circulation
- Published
- 2022-02-15
- Volume
- 145
- Issue
- 7
- Pages
- 513-530
- ISSN
- 0009-7322 (ISSN-L)
- 1524-4539
- PMC
- PMC8844107
- OpenAlex
- W4205450657
- Cited by
- 87
- References
- 86
- Citations by year
- 2026: 23 · 2025: 21 · 2024: 15 · 2023: 14 · 2022: 14
- FWCI
- 11.21
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Circulation (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Northwestern University
- National Heart, Lung, and Blood Institute (F31HL142223, R01HL089260, R01HL142935, T32HL007822, R00HL148542, R01HL132353, T32HL007444, R25HL145817)
- National Institute of General Medical Sciences (R01GM029090)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Valve Diseases and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Keywords
- aortic stenosis, sex differences, X chromosome inactivation escape, myofibroblast activation, valvular interstitial cells, BMX, STS, steroid sulfatase, endothelin-1, plasminogen activator inhibitor-1, extracellular matrix stiffness, valve fibrosis, sex as a biological variable
- MeSH terms
- Actins, Animals, Aortic Valve, Aortic Valve Stenosis, Cells, Cultured, Disease Models, Animal, Female, Gene Expression Regulation, Humans, Immunohistochemistry, Male, Sex Factors, Swine, Signal Transduction, Biomarkers, Gene Expression, X Chromosome Inactivation, Genes, X-Linked, Myofibroblasts, Transcriptome
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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