ERK hyperactivation in epidermal keratinocytes impairs intercellular adhesion and drives Grover disease pathology

Grover disease is an acquired epidermal blistering disorder in which keratinocytes lose intercellular connections. While its pathologic features are well defined, its etiology remains unclear, and there is no FDA-approved therapy. Interestingly, Grover disease was a common adverse event in clinical trials for cancer using B-RAF inhibitors, but it remained unknown how B-RAF blockade compromised skin integrity. Here, we identified ERK hyperactivation as a key driver of Grover disease pathology. We leveraged a fluorescent biosensor to confirm that the B-RAF inhibitors dabrafenib and vemurafenib paradoxically activated ERK in human keratinocytes and organotypic epidermis, disrupting cell-cell junctions and weakening epithelial integrity. Consistent with clinical data showing that concomitant MEK blockade prevents Grover disease in patients receiving B-RAF inhibitors, we found that MEK inhibition suppressed ERK and rescued cohesion of B-RAF-inhibited keratinocytes. Validating these results, we demonstrated ERK hyperactivation in patient biopsies from vemurafenib-induced Grover disease and from spontaneous Grover disease, revealing a common etiology for both. Finally, in line with our recent identification of ERK hyperactivation in Darier disease, a genetic disorder with identical pathology to Grover disease, our studies uncovered that the pathogenic mechanisms of these diseases converge on ERK signaling and support MEK inhibition as a therapeutic strategy.

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Publication Details

Journal
JCI Insight
Published
2024-09-26
DOI
https://doi.org/10.1172/jci.insight.182983
Citations
4
Primary Topic
Genetic and rare skin diseases.
Type
article
Field-Weighted Citation Impact
2.20

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article

ERK hyperactivation in epidermal keratinocytes impairs intercellular adhesion and drives Grover disease pathology

Cory L. Simpson, Shivam A. Zaver, Johann Eli Gudjonsson, Christopher J. Johnson et al.
4 citations
JCI Insight
Genetic and rare skin diseases.
2.20
article

ERK hyperactivation in epidermal keratinocytes impairs intercellular adhesion and drives Grover disease pathology

Cory L. Simpson, Shivam A. Zaver, Johann Eli Gudjonsson, Christopher J. Johnson, Afua Tiwaa, Emily Y. Chu, Paul W Harms
article en
4 citations

Abstract

Grover disease is an acquired epidermal blistering disorder in which keratinocytes lose intercellular connections. While its pathologic features are well defined, its etiology remains unclear, and there is no FDA-approved therapy. Interestingly, Grover disease was a common adverse event in clinical trials for cancer using B-RAF inhibitors, but it remained unknown how B-RAF blockade compromised skin integrity. Here, we identified ERK hyperactivation as a key driver of Grover disease pathology. We leveraged a fluorescent biosensor to confirm that the B-RAF inhibitors dabrafenib and vemurafenib paradoxically activated ERK in human keratinocytes and organotypic epidermis, disrupting cell-cell junctions and weakening epithelial integrity. Consistent with clinical data showing that concomitant MEK blockade prevents Grover disease in patients receiving B-RAF inhibitors, we found that MEK inhibition suppressed ERK and rescued cohesion of B-RAF-inhibited keratinocytes. Validating these results, we demonstrated ERK hyperactivation in patient biopsies from vemurafenib-induced Grover disease and from spontaneous Grover disease, revealing a common etiology for both. Finally, in line with our recent identification of ERK hyperactivation in Darier disease, a genetic disorder with identical pathology to Grover disease, our studies uncovered that the pathogenic mechanisms of these diseases converge on ERK signaling and support MEK inhibition as a therapeutic strategy.

JCI InsightVol. 9(21)
Virginia Mason Medical Center (US), University of Washington (US), University of Michigan (US), Hospital of the University of Pennsylvania (US), Michigan Medicine (US), Seattle University (US), University of Pennsylvania (US)
Foundation for Ichthyosis and Related Skin Types, A. Alfred Taubman Medical Research Institute, National Institute of Arthritis and Musculoskeletal and Skin Diseases
Zero hunger
Openalex Percentile: Top 12%
Genetic and rare skin diseases.
2.20
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