Intestinal BMP-9 locally upregulates FGF19 and is down-regulated in obese patients with diabetes

Bone morphogenetic protein (BMP)-9, a member of the TGFβ-family of cytokines, is believed to be mainly produced in the liver. The serum levels of BMP-9 were reported to be reduced in newly diagnosed diabetic patients and BMP-9 overexpression ameliorated steatosis in the high fat diet-induced obesity...

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Autores: Stephan Drexler, Cai, Chen, Hartmann, Anna-Lena, Moch, Denise, Gaitantzi, Haristi, Ney, Theresa, Kraemer, Malin, Chu, Yuan, Zheng, Yuwei, Rahbari, Mohammad, Treffs, Annalena, Reiser, Alena, Lenoir, Bénédicte, Valous, Nektarios A., Jäger, Dirk, Birgin, Emrullah, Sawant, Tejas A., Li, Qi, Xu, Keshu, Dong, Lingyue, Otto, Mirko, Itzel, Timo, Teufel, Andreas, Gretz, Norbert, Hawinkels, Lukas J.A.C., Sánchez Muñoz, Aranzazu, Herrera González, Blanca María, Schubert, Rudolf, Moshage, Han, Reissfelder, Christoph, Ebert, Matthias P.A., Rahbari, Nuh N., Breitkopf-Heinlein, Katja
Tipo de recurso: artículo
Fecha de publicación:2023
País:España
Institución:Universidad Complutense de Madrid (UCM)
Repositorio:Docta Complutense
Idioma:inglés
OAI Identifier:oai:docta.ucm.es:20.500.14352/107179
Acceso en línea:https://hdl.handle.net/20.500.14352/107179
Access Level:acceso abierto
Palabra clave:577.1
577.2
Diabetes
BMP-9
GDF2
Obesity
Liver steatosis
Biología molecular (Farmacia)
Bioquímica (Farmacia)
24 Ciencias de la Vida
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oai_identifier_str oai:docta.ucm.es:20.500.14352/107179
network_acronym_str ES
network_name_str España
repository_id_str
spelling Intestinal BMP-9 locally upregulates FGF19 and is down-regulated in obese patients with diabetesStephan DrexlerCai, ChenHartmann, Anna-LenaMoch, DeniseGaitantzi, HaristiNey, TheresaKraemer, MalinChu, YuanZheng, YuweiRahbari, MohammadTreffs, AnnalenaReiser, AlenaLenoir, BénédicteValous, Nektarios A.Jäger, DirkBirgin, EmrullahSawant, Tejas A.Li, QiXu, KeshuDong, LingyueOtto, MirkoItzel, TimoTeufel, AndreasGretz, NorbertHawinkels, Lukas J.A.C.Sánchez Muñoz, AranzazuHerrera González, Blanca MaríaSchubert, RudolfMoshage, HanReissfelder, ChristophEbert, Matthias P.A.Rahbari, Nuh N.Breitkopf-Heinlein, Katja577.1577.2DiabetesBMP-9GDF2ObesityLiver steatosisBiología molecular (Farmacia)Bioquímica (Farmacia)24 Ciencias de la VidaBone morphogenetic protein (BMP)-9, a member of the TGFβ-family of cytokines, is believed to be mainly produced in the liver. The serum levels of BMP-9 were reported to be reduced in newly diagnosed diabetic patients and BMP-9 overexpression ameliorated steatosis in the high fat diet-induced obesity mouse model. Furthermore, injection of BMP-9 in mice enhanced expression of fibroblast growth factor (FGF)21. However, whether BMP-9 also regulates the expression of the related FGF19 is not clear. Because both FGF21 and 19 were described to protect the liver from steatosis, we have further investigated the role of BMP-9 in this context. We first analyzed BMP-9 levels in the serum of streptozotocin (STZ)-induced diabetic rats (a model of type I diabetes) and confirmed that BMP-9 serum levels decrease during diabetes. Microarray analyses of RNA samples from hepatic and intestinal tissue from BMP-9 KO- and wild-type mice (C57/Bl6 background) pointed to basal expression of BMP-9 in both organs and revealed a down-regulation of hepatic Fgf21 and intestinal Fgf19 in the KO mice. Next, we analyzed BMP-9 levels in a cohort of obese patients with or without diabetes. Serum BMP-9 levels did not correlate with diabetes, but hepatic BMP-9 mRNA expression negatively correlated with steatosis in those patients that did not yet develop diabetes. Likewise, hepatic BMP-9 expression also negatively correlated with serum LPS levels. In situ hybridization analyses confirmed intestinal BMP-9 expression. Intestinal (but not hepatic) BMP-9 mRNA levels were decreased with diabetes and positively correlated with intestinal E-Cadherin expression. In vitro studies using organoids demonstrated that BMP-9 directly induces FGF19 in gut but not hepatocyte organoids, whereas no evidence of a direct induction of hepatic FGF21 by BMP-9 was found. Consistent with the in vitro data, a correlation between intestinal BMP-9 and FGF19 mRNA expression was seen in the patients’ samples. In summary, our data confirm that BMP-9 is involved in diabetes development in humans and in the control of the FGF-axis. More importantly, our data imply that not only hepatic but also intestinal BMP-9 associates with diabetes and steatosis development and controls FGF19 expression. The data support the conclusion that increased levels of BMP-9 would most likely be beneficial under pre-steatotic conditions, making supplementation of BMP-9 an interesting new approach for future therapies aiming at prevention of the development of a metabolic syndrome and liver steatosis.ElsevierUniversidad Complutense de Madrid20232023-01-0120232023-01-01journal articlehttp://purl.org/coar/resource_type/c_6501AMhttp://purl.org/coar/version/c_ab4af688f83e57aainfo:eu-repo/semantics/articleapplication/pdfhttps://hdl.handle.net/20.500.14352/107179reponame:Docta Complutenseinstname:Universidad Complutense de Madrid (UCM)Inglésengopen accesshttp://purl.org/coar/access_right/c_abf2Attribution-NonCommercial-NoDerivatives 4.0 Internationalhttp://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessoai:docta.ucm.es:20.500.14352/1071792026-06-02T12:44:21Z
dc.title.none.fl_str_mv Intestinal BMP-9 locally upregulates FGF19 and is down-regulated in obese patients with diabetes
title Intestinal BMP-9 locally upregulates FGF19 and is down-regulated in obese patients with diabetes
spellingShingle Intestinal BMP-9 locally upregulates FGF19 and is down-regulated in obese patients with diabetes
Stephan Drexler
577.1
577.2
Diabetes
BMP-9
GDF2
Obesity
Liver steatosis
Biología molecular (Farmacia)
Bioquímica (Farmacia)
24 Ciencias de la Vida
title_short Intestinal BMP-9 locally upregulates FGF19 and is down-regulated in obese patients with diabetes
title_full Intestinal BMP-9 locally upregulates FGF19 and is down-regulated in obese patients with diabetes
title_fullStr Intestinal BMP-9 locally upregulates FGF19 and is down-regulated in obese patients with diabetes
title_full_unstemmed Intestinal BMP-9 locally upregulates FGF19 and is down-regulated in obese patients with diabetes
title_sort Intestinal BMP-9 locally upregulates FGF19 and is down-regulated in obese patients with diabetes
dc.creator.none.fl_str_mv Stephan Drexler
Cai, Chen
Hartmann, Anna-Lena
Moch, Denise
Gaitantzi, Haristi
Ney, Theresa
Kraemer, Malin
Chu, Yuan
Zheng, Yuwei
Rahbari, Mohammad
Treffs, Annalena
Reiser, Alena
Lenoir, Bénédicte
Valous, Nektarios A.
Jäger, Dirk
Birgin, Emrullah
Sawant, Tejas A.
Li, Qi
Xu, Keshu
Dong, Lingyue
Otto, Mirko
Itzel, Timo
Teufel, Andreas
Gretz, Norbert
Hawinkels, Lukas J.A.C.
Sánchez Muñoz, Aranzazu
Herrera González, Blanca María
Schubert, Rudolf
Moshage, Han
Reissfelder, Christoph
Ebert, Matthias P.A.
Rahbari, Nuh N.
Breitkopf-Heinlein, Katja
author Stephan Drexler
author_facet Stephan Drexler
Cai, Chen
Hartmann, Anna-Lena
Moch, Denise
Gaitantzi, Haristi
Ney, Theresa
Kraemer, Malin
Chu, Yuan
Zheng, Yuwei
Rahbari, Mohammad
Treffs, Annalena
Reiser, Alena
Lenoir, Bénédicte
Valous, Nektarios A.
Jäger, Dirk
Birgin, Emrullah
Sawant, Tejas A.
Li, Qi
Xu, Keshu
Dong, Lingyue
Otto, Mirko
Itzel, Timo
Teufel, Andreas
Gretz, Norbert
Hawinkels, Lukas J.A.C.
Sánchez Muñoz, Aranzazu
Herrera González, Blanca María
Schubert, Rudolf
Moshage, Han
Reissfelder, Christoph
Ebert, Matthias P.A.
Rahbari, Nuh N.
Breitkopf-Heinlein, Katja
author_role author
author2 Cai, Chen
Hartmann, Anna-Lena
Moch, Denise
Gaitantzi, Haristi
Ney, Theresa
Kraemer, Malin
Chu, Yuan
Zheng, Yuwei
Rahbari, Mohammad
Treffs, Annalena
Reiser, Alena
Lenoir, Bénédicte
Valous, Nektarios A.
Jäger, Dirk
Birgin, Emrullah
Sawant, Tejas A.
Li, Qi
Xu, Keshu
Dong, Lingyue
Otto, Mirko
Itzel, Timo
Teufel, Andreas
Gretz, Norbert
Hawinkels, Lukas J.A.C.
Sánchez Muñoz, Aranzazu
Herrera González, Blanca María
Schubert, Rudolf
Moshage, Han
Reissfelder, Christoph
Ebert, Matthias P.A.
Rahbari, Nuh N.
Breitkopf-Heinlein, Katja
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universidad Complutense de Madrid
dc.subject.none.fl_str_mv 577.1
577.2
Diabetes
BMP-9
GDF2
Obesity
Liver steatosis
Biología molecular (Farmacia)
Bioquímica (Farmacia)
24 Ciencias de la Vida
topic 577.1
577.2
Diabetes
BMP-9
GDF2
Obesity
Liver steatosis
Biología molecular (Farmacia)
Bioquímica (Farmacia)
24 Ciencias de la Vida
description Bone morphogenetic protein (BMP)-9, a member of the TGFβ-family of cytokines, is believed to be mainly produced in the liver. The serum levels of BMP-9 were reported to be reduced in newly diagnosed diabetic patients and BMP-9 overexpression ameliorated steatosis in the high fat diet-induced obesity mouse model. Furthermore, injection of BMP-9 in mice enhanced expression of fibroblast growth factor (FGF)21. However, whether BMP-9 also regulates the expression of the related FGF19 is not clear. Because both FGF21 and 19 were described to protect the liver from steatosis, we have further investigated the role of BMP-9 in this context. We first analyzed BMP-9 levels in the serum of streptozotocin (STZ)-induced diabetic rats (a model of type I diabetes) and confirmed that BMP-9 serum levels decrease during diabetes. Microarray analyses of RNA samples from hepatic and intestinal tissue from BMP-9 KO- and wild-type mice (C57/Bl6 background) pointed to basal expression of BMP-9 in both organs and revealed a down-regulation of hepatic Fgf21 and intestinal Fgf19 in the KO mice. Next, we analyzed BMP-9 levels in a cohort of obese patients with or without diabetes. Serum BMP-9 levels did not correlate with diabetes, but hepatic BMP-9 mRNA expression negatively correlated with steatosis in those patients that did not yet develop diabetes. Likewise, hepatic BMP-9 expression also negatively correlated with serum LPS levels. In situ hybridization analyses confirmed intestinal BMP-9 expression. Intestinal (but not hepatic) BMP-9 mRNA levels were decreased with diabetes and positively correlated with intestinal E-Cadherin expression. In vitro studies using organoids demonstrated that BMP-9 directly induces FGF19 in gut but not hepatocyte organoids, whereas no evidence of a direct induction of hepatic FGF21 by BMP-9 was found. Consistent with the in vitro data, a correlation between intestinal BMP-9 and FGF19 mRNA expression was seen in the patients’ samples. In summary, our data confirm that BMP-9 is involved in diabetes development in humans and in the control of the FGF-axis. More importantly, our data imply that not only hepatic but also intestinal BMP-9 associates with diabetes and steatosis development and controls FGF19 expression. The data support the conclusion that increased levels of BMP-9 would most likely be beneficial under pre-steatotic conditions, making supplementation of BMP-9 an interesting new approach for future therapies aiming at prevention of the development of a metabolic syndrome and liver steatosis.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023-01-01
2023
2023-01-01
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
AM
http://purl.org/coar/version/c_ab4af688f83e57aa
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://hdl.handle.net/20.500.14352/107179
url https://hdl.handle.net/20.500.14352/107179
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
Attribution-NonCommercial-NoDerivatives 4.0 International
http://creativecommons.org/licenses/by-nc-nd/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
Attribution-NonCommercial-NoDerivatives 4.0 International
http://creativecommons.org/licenses/by-nc-nd/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:Docta Complutense
instname:Universidad Complutense de Madrid (UCM)
instname_str Universidad Complutense de Madrid (UCM)
reponame_str Docta Complutense
collection Docta Complutense
repository.name.fl_str_mv
repository.mail.fl_str_mv
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