Tricyclic antidepressants target FKBP51 SUMOylation to restore glucocorticoid receptor activity

FKBP51 is an important inhibitor of the glucocorticoid receptor (GR) signaling. High FKBP51 levels are associated to stress-related disorders, which are linked to GR resistance. SUMO conjugation to FKBP51 is necessary for FKBP51’s inhibitory action on GR. The GR/FKBP51 pathway is target of antidepre...

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Published inMolecular psychiatry Vol. 27; no. 5; pp. 2533 - 2545
Main Authors Budziñski, Maia L., Sokn, Clara, Gobbini, Romina, Ugo, Belén, Antunica-Noguerol, María, Senin, Sergio, Bajaj, Thomas, Gassen, Nils C., Rein, Theo, Schmidt, Mathias V., Binder, Elisabeth B., Arzt, Eduardo, Liberman, Ana C.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.05.2022
Nature Publishing Group
Subjects
13/109
13/95
38/77
42/89
631/337
631/378
631/45
631/80
82/83
96/106
Animals
Antidepressants
Antidepressive Agents, Tricyclic - pharmacology
Astrocytes
Behavioral Sciences
Biological Psychology
Clomipramine
Gene Expression Regulation
Glucocorticoids
Hsp90 protein
Medicine
Medicine & Public Health
Mice
Neurosciences
Pharmacotherapy
Psychiatry
Rats
Receptors, Glucocorticoid - metabolism
Repressors
SUMO protein
Sumoylation
Tacrolimus Binding Proteins - metabolism
Tricyclic antidepressants
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Abstract FKBP51 is an important inhibitor of the glucocorticoid receptor (GR) signaling. High FKBP51 levels are associated to stress-related disorders, which are linked to GR resistance. SUMO conjugation to FKBP51 is necessary for FKBP51’s inhibitory action on GR. The GR/FKBP51 pathway is target of antidepressant action. Thus we investigated if these drugs could inhibit FKBP51 SUMOylation and therefore restore GR activity. Screening cells using Ni 2+ affinity and in vitro SUMOylation assays revealed that tricyclic antidepressants- particularly clomipramine- inhibited FKBP51 SUMOylation. Our data show that clomipramine binds to FKBP51 inhibiting its interaction with PIAS4 and therefore hindering its SUMOylation. The inhibition of FKBP51 SUMOylation decreased its binding to Hsp90 and GR facilitating FKBP52 recruitment, and enhancing GR activity. Reduction of PIAS4 expression in rat primary astrocytes impaired FKBP51 interaction with GR, while clomipramine could no longer exert its inhibitory action. This mechanism was verified in vivo in mice treated with clomipramine. These results describe the action of antidepressants as repressors of FKBP51 SUMOylation as a molecular switch for restoring GR sensitivity, thereby providing new potential routes of antidepressant intervention.
AbstractList FKBP51 is an important inhibitor of the glucocorticoid receptor (GR) signaling. High FKBP51 levels are associated to stress-related disorders, which are linked to GR resistance. SUMO conjugation to FKBP51 is necessary for FKBP51’s inhibitory action on GR. The GR/FKBP51 pathway is target of antidepressant action. Thus we investigated if these drugs could inhibit FKBP51 SUMOylation and therefore restore GR activity. Screening cells using Ni 2+ affinity and in vitro SUMOylation assays revealed that tricyclic antidepressants- particularly clomipramine- inhibited FKBP51 SUMOylation. Our data show that clomipramine binds to FKBP51 inhibiting its interaction with PIAS4 and therefore hindering its SUMOylation. The inhibition of FKBP51 SUMOylation decreased its binding to Hsp90 and GR facilitating FKBP52 recruitment, and enhancing GR activity. Reduction of PIAS4 expression in rat primary astrocytes impaired FKBP51 interaction with GR, while clomipramine could no longer exert its inhibitory action. This mechanism was verified in vivo in mice treated with clomipramine. These results describe the action of antidepressants as repressors of FKBP51 SUMOylation as a molecular switch for restoring GR sensitivity, thereby providing new potential routes of antidepressant intervention.
FKBP51 is an important inhibitor of the glucocorticoid receptor (GR) signaling. High FKBP51 levels are associated to stress-related disorders, which are linked to GR resistance. SUMO conjugation to FKBP51 is necessary for FKBP51’s inhibitory action on GR. The GR/FKBP51 pathway is target of antidepressant action. Thus we investigated if these drugs could inhibit FKBP51 SUMOylation and therefore restore GR activity. Screening cells using Ni2+ affinity and in vitro SUMOylation assays revealed that tricyclic antidepressants- particularly clomipramine- inhibited FKBP51 SUMOylation. Our data show that clomipramine binds to FKBP51 inhibiting its interaction with PIAS4 and therefore hindering its SUMOylation. The inhibition of FKBP51 SUMOylation decreased its binding to Hsp90 and GR facilitating FKBP52 recruitment, and enhancing GR activity. Reduction of PIAS4 expression in rat primary astrocytes impaired FKBP51 interaction with GR, while clomipramine could no longer exert its inhibitory action. This mechanism was verified in vivo in mice treated with clomipramine. These results describe the action of antidepressants as repressors of FKBP51 SUMOylation as a molecular switch for restoring GR sensitivity, thereby providing new potential routes of antidepressant intervention.
FKBP51 is an important inhibitor of the glucocorticoid receptor (GR) signaling. High FKBP51 levels are associated to stress-related disorders, which are linked to GR resistance. SUMO conjugation to FKBP51 is necessary for FKBP51's inhibitory action on GR. The GR/FKBP51 pathway is target of antidepressant action. Thus we investigated if these drugs could inhibit FKBP51 SUMOylation and therefore restore GR activity. Screening cells using Ni affinity and in vitro SUMOylation assays revealed that tricyclic antidepressants- particularly clomipramine- inhibited FKBP51 SUMOylation. Our data show that clomipramine binds to FKBP51 inhibiting its interaction with PIAS4 and therefore hindering its SUMOylation. The inhibition of FKBP51 SUMOylation decreased its binding to Hsp90 and GR facilitating FKBP52 recruitment, and enhancing GR activity. Reduction of PIAS4 expression in rat primary astrocytes impaired FKBP51 interaction with GR, while clomipramine could no longer exert its inhibitory action. This mechanism was verified in vivo in mice treated with clomipramine. These results describe the action of antidepressants as repressors of FKBP51 SUMOylation as a molecular switch for restoring GR sensitivity, thereby providing new potential routes of antidepressant intervention.
Author Binder, Elisabeth B.
Budziñski, Maia L.
Rein, Theo
Gassen, Nils C.
Arzt, Eduardo
Liberman, Ana C.
Gobbini, Romina
Schmidt, Mathias V.
Ugo, Belén
Antunica-Noguerol, María
Sokn, Clara
Senin, Sergio
Bajaj, Thomas
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  surname: Schmidt
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Snippet FKBP51 is an important inhibitor of the glucocorticoid receptor (GR) signaling. High FKBP51 levels are associated to stress-related disorders, which are linked...
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SubjectTerms 13/109
13/95
38/77
42/89
631/337
631/378
631/45
631/80
82/83
96/106
Animals
Antidepressants
Antidepressive Agents, Tricyclic - pharmacology
Astrocytes
Behavioral Sciences
Biological Psychology
Clomipramine
Gene Expression Regulation
Glucocorticoids
Hsp90 protein
Medicine
Medicine & Public Health
Mice
Neurosciences
Pharmacotherapy
Psychiatry
Rats
Receptors, Glucocorticoid - metabolism
Repressors
SUMO protein
Sumoylation
Tacrolimus Binding Proteins - metabolism
Tricyclic antidepressants
Title Tricyclic antidepressants target FKBP51 SUMOylation to restore glucocorticoid receptor activity
URI https://link.springer.com/article/10.1038/s41380-022-01491-0
https://www.ncbi.nlm.nih.gov/pubmed/35256747
https://www.proquest.com/docview/2669793767
https://search.proquest.com/docview/2637315449
Volume 27
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