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[Preprint]. 2025 Aug 25:2024.11.14.623646. Originally published 2024 Nov 15. [Version 2] doi: 10.1101/2024.11.14.623646

ATF4 regulates mitochondrial dysfunction and mitophagy, contributing to corneal endothelial apoptosis in Fuchs’ dystrophy

Saba Qureshi, Stefan Y Kim, Stephanie Lee, Lukas Ritzer, William Steidl, Gayle Joliet Krest, Anisha Kasi, Varun Kumar
PMCID: PMC11577245  PMID: 39569143

Abstract

PURPOSE

Endoplasmic reticulum (ER) stress, mitochondrial dysfunction, and mitophagy are known to contribute independently to corneal endothelial cell (CEnC) apoptosis in Fuchs’ endothelial corneal dystrophy (FECD). However, the role of a specific ER stress pathway (PERK-ATF4-CHOP) in regulating these events is unknown. This study aims to investigate the role of ATF4 in regulating mitochondrial dysfunction and mitophagy, which ultimately leads to CEnC apoptosis in FECD.

METHODS

Human corneal endothelial cell line (21T), Fuchs’ corneal endothelial cell line (F35T), and primary human corneal endothelial cells were treated with ER stressor tunicamycin (Tun). ATF4 siRNA was used to knock down ATF4 in 21T cell line and primary corneal endothelial cells. Mitophagy and apoptotic proteins were analyzed using Western blotting. ATF4 +/- and ATF4 +/+ mice were irradiated with UVA to assess ER stress and corneal endothelial apoptosis.

RESULTS

F35T cell line had significantly increased expression of the ER stress pathway as well as caspase-mediated apoptotic molecules compared to 21T at baseline, which further increased after tunicamycin treatment. F35T cells exhibited significantly decreased ATP and MMP, and increased mitochondrial fragmentation, which was further exacerbated after Tunicamycin. F35T cell line also demonstrated inhibition of mitophagy, similar to 21T, after treatment with Tunicamycin, despite the upregulation of mitophagy initiators. ATF4 knockdown attenuated ER and mitochondrial stress proteins, rescued mitochondrial membrane potential (MMP) loss, downregulated mitochondrial fragmentation, activated mitophagy, and prevented cell death under chronic ER stress. ATF4 +/- mice had increased CE numbers, with improved cellular morphology and decreased ER stress CHOP expression, compared to ATF4+/+ mice post-UVA.

CONCLUSIONS

Pro-apoptotic ATF4 induction following ER stress disrupts mitochondrial function, leading to mitophagy inhibition and CEnC apoptosis. This study highlights the importance of ATF4 in ER-mitochondrial crosstalk and its contribution to CEnC apoptosis in FECD.

Full Text Availability

The license terms selected by the author(s) for this preprint version do not permit archiving in PMC. The full text is available from the preprint server.


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