Renal interstitial fibroblasts coproduce erythropoietin and renin under anaemic conditions.


Journal

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

Informations de publication

Date de publication:
Feb 2021
Historique:
received: 03 04 2020
revised: 08 12 2020
accepted: 04 01 2021
pubmed: 29 1 2021
medline: 14 10 2021
entrez: 28 1 2021
Statut: ppublish

Résumé

Erythrocyte mass contributes to maintaining systemic oxygen delivery and blood viscosity, with the latter being one of the determinants of blood pressure. However, the physiological response to blood pressure changes under anaemic conditions remain unknown. We show that anaemia decreases blood pressure in human patients and mouse models. Analyses of pathways related to blood pressure regulation demonstrate that anaemia enhances the expression of the gene encoding the vasopressor substance renin in kidneys. Although kidney juxtaglomerular cells are known to continuously produce renin, renal interstitial fibroblasts are identified in the present study as a novel site of renin induction under anaemic hypotensive conditions in mice and rats. Notably, some renal interstitial fibroblasts are found to simultaneously express renin and the erythroid growth factor erythropoietin in the anaemic mouse kidney. Antihypertensive agents but not hypoxic stimuli induced interstitial renin expression, suggesting that blood pressure reduction triggers interstitial renin induction in anaemic mice. The interstitial renin expression was also detected in injured fibrotic kidneys of the mouse and human, and the renin-expressing interstitial cells in murine fibrotic kidneys were identified as myofibroblasts originating from renal interstitial fibroblasts. Since the elevated expression levels of renin in fibrotic kidneys along with progression of renal fibrosis were well correlated to the systemic blood pressure increase, the renal interstitial renin production seemed to affect systemic blood pressure. Renal interstitial fibroblasts function as central controllers of systemic oxygen delivery by producing both renin and erythropoietin. Grants-in-Aid from Japan Society for the Promotion of Science (JSPS) KAKENHI (17K19680, 15H04691, and 26111002) and the Takeda Science Foundation.

Sections du résumé

BACKGROUND BACKGROUND
Erythrocyte mass contributes to maintaining systemic oxygen delivery and blood viscosity, with the latter being one of the determinants of blood pressure. However, the physiological response to blood pressure changes under anaemic conditions remain unknown.
METHODS AND FINDINGS RESULTS
We show that anaemia decreases blood pressure in human patients and mouse models. Analyses of pathways related to blood pressure regulation demonstrate that anaemia enhances the expression of the gene encoding the vasopressor substance renin in kidneys. Although kidney juxtaglomerular cells are known to continuously produce renin, renal interstitial fibroblasts are identified in the present study as a novel site of renin induction under anaemic hypotensive conditions in mice and rats. Notably, some renal interstitial fibroblasts are found to simultaneously express renin and the erythroid growth factor erythropoietin in the anaemic mouse kidney. Antihypertensive agents but not hypoxic stimuli induced interstitial renin expression, suggesting that blood pressure reduction triggers interstitial renin induction in anaemic mice. The interstitial renin expression was also detected in injured fibrotic kidneys of the mouse and human, and the renin-expressing interstitial cells in murine fibrotic kidneys were identified as myofibroblasts originating from renal interstitial fibroblasts. Since the elevated expression levels of renin in fibrotic kidneys along with progression of renal fibrosis were well correlated to the systemic blood pressure increase, the renal interstitial renin production seemed to affect systemic blood pressure.
INTERPRETATION CONCLUSIONS
Renal interstitial fibroblasts function as central controllers of systemic oxygen delivery by producing both renin and erythropoietin.
FUNDING BACKGROUND
Grants-in-Aid from Japan Society for the Promotion of Science (JSPS) KAKENHI (17K19680, 15H04691, and 26111002) and the Takeda Science Foundation.

Identifiants

pubmed: 33508746
pii: S2352-3964(21)00002-5
doi: 10.1016/j.ebiom.2021.103209
pmc: PMC7841315
pii:
doi:

Substances chimiques

Biomarkers 0
Erythropoietin 11096-26-7
Renin EC 3.4.23.15

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

103209

Informations de copyright

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

Déclaration de conflit d'intérêts

Declaration of Competing Interests The authors declare no competing interests.

Auteurs

Kenichiro Miyauchi (K)

Division of Oxygen Biology, United Centres for Advanced Research and Translational Medicine, Tohoku University Graduate School of Medicine, Seiryo-machi 2-1, Aoba-ku, Sendai, Miyagi 980-8575, Japan; Division of Nephrology, Endocrinology, and Vascular Medicine, Tohoku University Graduate School of Medicine, Japan.

Taku Nakai (T)

Division of Oxygen Biology, United Centres for Advanced Research and Translational Medicine, Tohoku University Graduate School of Medicine, Seiryo-machi 2-1, Aoba-ku, Sendai, Miyagi 980-8575, Japan.

Sakae Saito (S)

Tohoku Medical Megabank Organization, Tohoku University Graduate School of Medicine, Seiryo-machi 2-1, Aoba-ku, Sendai, Miyagi 980-8575, Japan.

Tae Yamamoto (T)

Division of Nephrology, Endocrinology, and Vascular Medicine, Tohoku University Graduate School of Medicine, Japan.

Koji Sato (K)

Division of Oxygen Biology, United Centres for Advanced Research and Translational Medicine, Tohoku University Graduate School of Medicine, Seiryo-machi 2-1, Aoba-ku, Sendai, Miyagi 980-8575, Japan; Division of Nephrology, Endocrinology, and Vascular Medicine, Tohoku University Graduate School of Medicine, Japan.

Koichiro Kato (K)

Division of Oxygen Biology, United Centres for Advanced Research and Translational Medicine, Tohoku University Graduate School of Medicine, Seiryo-machi 2-1, Aoba-ku, Sendai, Miyagi 980-8575, Japan.

Masahiro Nezu (M)

Division of Oxygen Biology, United Centres for Advanced Research and Translational Medicine, Tohoku University Graduate School of Medicine, Seiryo-machi 2-1, Aoba-ku, Sendai, Miyagi 980-8575, Japan; Division of Nephrology, Endocrinology, and Vascular Medicine, Tohoku University Graduate School of Medicine, Japan; Tohoku Medical Megabank Organization, Tohoku University Graduate School of Medicine, Seiryo-machi 2-1, Aoba-ku, Sendai, Miyagi 980-8575, Japan.

Mariko Miyazaki (M)

Division of Nephrology, Endocrinology, and Vascular Medicine, Tohoku University Graduate School of Medicine, Japan.

Sadayoshi Ito (S)

Division of Nephrology, Endocrinology, and Vascular Medicine, Tohoku University Graduate School of Medicine, Japan.

Masayuki Yamamoto (M)

Tohoku Medical Megabank Organization, Tohoku University Graduate School of Medicine, Seiryo-machi 2-1, Aoba-ku, Sendai, Miyagi 980-8575, Japan.

Norio Suzuki (N)

Division of Oxygen Biology, United Centres for Advanced Research and Translational Medicine, Tohoku University Graduate School of Medicine, Seiryo-machi 2-1, Aoba-ku, Sendai, Miyagi 980-8575, Japan. Electronic address: sunorio@med.tohoku.ac.jp.

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Classifications MeSH