Deiodinase-3 is a thyrostat to regulate podocyte homeostasis.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Oct 2021
Historique:
received: 17 06 2021
revised: 22 09 2021
accepted: 22 09 2021
pubmed: 15 10 2021
medline: 8 2 2022
entrez: 14 10 2021
Statut: ppublish

Résumé

Nephrotic syndrome (NS) is associated with kidney podocyte injury and may occur as part of thyroid autoimmunity such as Graves' disease. Therefore, the present study was designed to ascertain if and how podocytes respond to and regulate the input of biologically active thyroid hormone (TH), 3,5,3'-triiodothyronine (T3); and also to decipher the pathophysiological role of type 3 deiodinase (D3), a membrane-bound selenoenzyme that inactivates TH, in kidney disease. To study D3 function in healthy and injured (PAN, puromycin aminonucleoside and LPS, Lipopolysaccharide-mediated) podocytes, immunofluorescence, qPCR and podocyte-specific D3 knockout mouse were used. Surface plasmon resonance (SPR), co-immunoprecipitation and Proximity Ligation Assay (PLA) were used for the interaction studies. Healthy podocytes expressed D3 as the predominant deiodinase isoform. Upon podocyte injury, levels of Dio3 transcript and D3 protein were dramatically reduced both in vitro and in the LPS mouse model of podocyte damage. D3 was no longer directed to the cell membrane, it accumulated in the Golgi and nucleus instead. Further, depleting D3 from the mouse podocytes resulted in foot process effacement and proteinuria. Treatment of mouse podocytes with T3 phenocopied the absence of D3 and elicited activation of αvβ3 integrin signaling, which led to podocyte injury. We also confirmed presence of an active thyroid stimulating hormone receptor (TSH-R) on mouse podocytes, engagement and activation of which resulted in podocyte injury. The study provided a mechanistic insight into how D3-αvβ3 integrin interaction can minimize T3-dependent integrin activation, illustrating how D3 could act as a renoprotective thyrostat in podocytes. Further, injury caused by binding of TSH-R with TSH-R antibody, as found in patients with Graves' disease, explained a plausible link between thyroid disorder and NS. This work was supported by American Thyroid Association (ATA-2018-050.R1).

Sections du résumé

BACKGROUND BACKGROUND
Nephrotic syndrome (NS) is associated with kidney podocyte injury and may occur as part of thyroid autoimmunity such as Graves' disease. Therefore, the present study was designed to ascertain if and how podocytes respond to and regulate the input of biologically active thyroid hormone (TH), 3,5,3'-triiodothyronine (T3); and also to decipher the pathophysiological role of type 3 deiodinase (D3), a membrane-bound selenoenzyme that inactivates TH, in kidney disease.
METHODS METHODS
To study D3 function in healthy and injured (PAN, puromycin aminonucleoside and LPS, Lipopolysaccharide-mediated) podocytes, immunofluorescence, qPCR and podocyte-specific D3 knockout mouse were used. Surface plasmon resonance (SPR), co-immunoprecipitation and Proximity Ligation Assay (PLA) were used for the interaction studies.
FINDINGS RESULTS
Healthy podocytes expressed D3 as the predominant deiodinase isoform. Upon podocyte injury, levels of Dio3 transcript and D3 protein were dramatically reduced both in vitro and in the LPS mouse model of podocyte damage. D3 was no longer directed to the cell membrane, it accumulated in the Golgi and nucleus instead. Further, depleting D3 from the mouse podocytes resulted in foot process effacement and proteinuria. Treatment of mouse podocytes with T3 phenocopied the absence of D3 and elicited activation of αvβ3 integrin signaling, which led to podocyte injury. We also confirmed presence of an active thyroid stimulating hormone receptor (TSH-R) on mouse podocytes, engagement and activation of which resulted in podocyte injury.
INTERPRETATION CONCLUSIONS
The study provided a mechanistic insight into how D3-αvβ3 integrin interaction can minimize T3-dependent integrin activation, illustrating how D3 could act as a renoprotective thyrostat in podocytes. Further, injury caused by binding of TSH-R with TSH-R antibody, as found in patients with Graves' disease, explained a plausible link between thyroid disorder and NS.
FUNDING BACKGROUND
This work was supported by American Thyroid Association (ATA-2018-050.R1).

Identifiants

pubmed: 34649077
pii: S2352-3964(21)00410-2
doi: 10.1016/j.ebiom.2021.103617
pmc: PMC8517284
pii:
doi:

Substances chimiques

Integrin alphaVbeta3 0
Receptors, Thyrotropin 0
Thyroid Hormones 0
Triiodothyronine 06LU7C9H1V
Puromycin Aminonucleoside 58-60-6
iodothyronine deiodinase type III EC 1.11.1.-
Iodide Peroxidase EC 1.11.1.8

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

103617

Subventions

Organisme : NIDDK NIH HHS
ID : R01 DK077148
Pays : United States

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest Jochen Reiser has patents on novel strategies for kidney therapeutics and stands to gain royalties from their commercialization. He is the co-founder of Walden Biosciences (Cambridge, MA, USA), a biotechnology company in which he has financial interest, including stock. Antonio Bianco is a consultant for Synthonics, Allergan, Abbvie, and BLA Technology. Other authors have nothing to disclose and there are no competing or conflicting interests.

Auteurs

Shivangi Agarwal (S)

Department of Internal Medicine, Rush University, Chicago, IL 60612.

Kwi Hye Koh (KH)

Department of Internal Medicine, Rush University, Chicago, IL 60612.

Nicholas J Tardi (NJ)

Department of Internal Medicine, Rush University, Chicago, IL 60612.

Chuang Chen (C)

Department of Internal Medicine, Rush University, Chicago, IL 60612.

Ranadheer Reddy Dande (RR)

Department of Internal Medicine, Rush University, Chicago, IL 60612.

Joao Pedro WerneckdeCastro (JP)

Department of Internal Medicine, Rush University, Chicago, IL 60612.

Yashwanth Reddy Sudhini (YR)

Department of Internal Medicine, Rush University, Chicago, IL 60612.

Cristina Luongo (C)

Department of Public Health, University of Naples "Federico II," Naples, Italy.

Domenico Salvatore (D)

Department of Public Health, University of Naples "Federico II," Naples, Italy.

Beata Samelko (B)

Department of Internal Medicine, Rush University, Chicago, IL 60612.

Mehmet M Altintas (MM)

Department of Internal Medicine, Rush University, Chicago, IL 60612.

Steve Mangos (S)

Department of Internal Medicine, Rush University, Chicago, IL 60612.

Antonio Bianco (A)

Department of Medicine, University of Chicago, Chicago, IL 60637.

Jochen Reiser (J)

Department of Internal Medicine, Rush University, Chicago, IL 60612. Electronic address: jochen_reiser@rush.edu.

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Classifications MeSH