Vasoactive intestinal peptide promotes secretory differentiation and mitigates radiation-induced intestinal injury
Background Vasoactive intestinal peptide (VIP) is a neuronal peptide with prominent distribution along the enteric nervous system. While effects of VIP on intestinal motility, mucosal vasodilation, secretion, and mucosal immune cell function are well-studied, the direct impact of VIP on intestinal e...
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| Published in: | Stem cell research & therapy Vol. 15; no. 1; pp. 348 - 14 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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BioMed Central
08.10.2024
BioMed Central Ltd BMC |
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| ISSN: | 1757-6512, 1757-6512 |
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| Abstract | Background
Vasoactive intestinal peptide (VIP) is a neuronal peptide with prominent distribution along the enteric nervous system. While effects of VIP on intestinal motility, mucosal vasodilation, secretion, and mucosal immune cell function are well-studied, the direct impact of VIP on intestinal epithelial cell turnover and differentiation remains less understood. Intestinal stem and progenitor cells are essential for the maintenance of intestinal homeostasis and regeneration, and their functions can be modulated by factors of the stem cell niche, including neuronal mediators. Here, we investigated the role of VIP in regulating intestinal epithelial homeostasis and regeneration following irradiation-induced injury.
Methods
Jejunal organoids were derived from male and female C57Bl6/J,
Lgr5
-EGFP-IRES-CreER
T2
or
Lgr5
-EGFP-IRES-CreER
T2
/
R26
R-LSL-TdTomato mice and treated with VIP prior to analysis. Injury conditions were induced by exposing organoids to 6 Gy of irradiation (IR). To investigate protective effects of VIP in vivo, mice received 12 Gy of abdominal IR followed by intraperitoneal injections of VIP.
Results
We observed that VIP promotes epithelial differentiation towards a secretory phenotype predominantly via the p38 MAPK pathway. Moreover, VIP prominently modulated epithelial proliferation as well as the number and proliferative activity of Lgr5-EGFP
+
progenitor cells under homeostatic conditions. In the context of acute irradiation injury in vitro, we observed that IR injury renders Lgr5-EGFP
+
progenitor cells more susceptible to VIP-induced modulations, which coincided with the strong promotion of epithelial regeneration by VIP. Finally, the observed effects translate into an in vivo model of abdominal irradiation, where VIP showed to prominently mitigate radiation-induced injury.
Conclusions
VIP prominently governs intestinal homeostasis by regulating epithelial progenitor cell proliferation and differentiation and promotes intestinal regeneration following acute irradiation injury. |
|---|---|
| AbstractList | Abstract Background Vasoactive intestinal peptide (VIP) is a neuronal peptide with prominent distribution along the enteric nervous system. While effects of VIP on intestinal motility, mucosal vasodilation, secretion, and mucosal immune cell function are well-studied, the direct impact of VIP on intestinal epithelial cell turnover and differentiation remains less understood. Intestinal stem and progenitor cells are essential for the maintenance of intestinal homeostasis and regeneration, and their functions can be modulated by factors of the stem cell niche, including neuronal mediators. Here, we investigated the role of VIP in regulating intestinal epithelial homeostasis and regeneration following irradiation-induced injury. Methods Jejunal organoids were derived from male and female C57Bl6/J, Lgr5-EGFP-IRES-CreERT2 or Lgr5-EGFP-IRES-CreERT2/R26R-LSL-TdTomato mice and treated with VIP prior to analysis. Injury conditions were induced by exposing organoids to 6 Gy of irradiation (IR). To investigate protective effects of VIP in vivo, mice received 12 Gy of abdominal IR followed by intraperitoneal injections of VIP. Results We observed that VIP promotes epithelial differentiation towards a secretory phenotype predominantly via the p38 MAPK pathway. Moreover, VIP prominently modulated epithelial proliferation as well as the number and proliferative activity of Lgr5-EGFP+ progenitor cells under homeostatic conditions. In the context of acute irradiation injury in vitro, we observed that IR injury renders Lgr5-EGFP+ progenitor cells more susceptible to VIP-induced modulations, which coincided with the strong promotion of epithelial regeneration by VIP. Finally, the observed effects translate into an in vivo model of abdominal irradiation, where VIP showed to prominently mitigate radiation-induced injury. Conclusions VIP prominently governs intestinal homeostasis by regulating epithelial progenitor cell proliferation and differentiation and promotes intestinal regeneration following acute irradiation injury. Background Vasoactive intestinal peptide (VIP) is a neuronal peptide with prominent distribution along the enteric nervous system. While effects of VIP on intestinal motility, mucosal vasodilation, secretion, and mucosal immune cell function are well-studied, the direct impact of VIP on intestinal epithelial cell turnover and differentiation remains less understood. Intestinal stem and progenitor cells are essential for the maintenance of intestinal homeostasis and regeneration, and their functions can be modulated by factors of the stem cell niche, including neuronal mediators. Here, we investigated the role of VIP in regulating intestinal epithelial homeostasis and regeneration following irradiation-induced injury. Methods Jejunal organoids were derived from male and female C57Bl6/J, Lgr5 -EGFP-IRES-CreER T2 or Lgr5 -EGFP-IRES-CreER T2 / R26 R-LSL-TdTomato mice and treated with VIP prior to analysis. Injury conditions were induced by exposing organoids to 6 Gy of irradiation (IR). To investigate protective effects of VIP in vivo, mice received 12 Gy of abdominal IR followed by intraperitoneal injections of VIP. Results We observed that VIP promotes epithelial differentiation towards a secretory phenotype predominantly via the p38 MAPK pathway. Moreover, VIP prominently modulated epithelial proliferation as well as the number and proliferative activity of Lgr5-EGFP + progenitor cells under homeostatic conditions. In the context of acute irradiation injury in vitro, we observed that IR injury renders Lgr5-EGFP + progenitor cells more susceptible to VIP-induced modulations, which coincided with the strong promotion of epithelial regeneration by VIP. Finally, the observed effects translate into an in vivo model of abdominal irradiation, where VIP showed to prominently mitigate radiation-induced injury. Conclusions VIP prominently governs intestinal homeostasis by regulating epithelial progenitor cell proliferation and differentiation and promotes intestinal regeneration following acute irradiation injury. Background Vasoactive intestinal peptide (VIP) is a neuronal peptide with prominent distribution along the enteric nervous system. While effects of VIP on intestinal motility, mucosal vasodilation, secretion, and mucosal immune cell function are well-studied, the direct impact of VIP on intestinal epithelial cell turnover and differentiation remains less understood. Intestinal stem and progenitor cells are essential for the maintenance of intestinal homeostasis and regeneration, and their functions can be modulated by factors of the stem cell niche, including neuronal mediators. Here, we investigated the role of VIP in regulating intestinal epithelial homeostasis and regeneration following irradiation-induced injury. Methods Jejunal organoids were derived from male and female C57Bl6/J, Lgr5-EGFP-IRES-CreER.sup.T2 or Lgr5-EGFP-IRES-CreER.sup.T2/R26R-LSL-TdTomato mice and treated with VIP prior to analysis. Injury conditions were induced by exposing organoids to 6 Gy of irradiation (IR). To investigate protective effects of VIP in vivo, mice received 12 Gy of abdominal IR followed by intraperitoneal injections of VIP. Results We observed that VIP promotes epithelial differentiation towards a secretory phenotype predominantly via the p38 MAPK pathway. Moreover, VIP prominently modulated epithelial proliferation as well as the number and proliferative activity of Lgr5-EGFP.sup.+ progenitor cells under homeostatic conditions. In the context of acute irradiation injury in vitro, we observed that IR injury renders Lgr5-EGFP.sup.+ progenitor cells more susceptible to VIP-induced modulations, which coincided with the strong promotion of epithelial regeneration by VIP. Finally, the observed effects translate into an in vivo model of abdominal irradiation, where VIP showed to prominently mitigate radiation-induced injury. Conclusions VIP prominently governs intestinal homeostasis by regulating epithelial progenitor cell proliferation and differentiation and promotes intestinal regeneration following acute irradiation injury. Keywords: VIP, Intestinal progenitor cells, Irradiation, Regeneration Vasoactive intestinal peptide (VIP) is a neuronal peptide with prominent distribution along the enteric nervous system. While effects of VIP on intestinal motility, mucosal vasodilation, secretion, and mucosal immune cell function are well-studied, the direct impact of VIP on intestinal epithelial cell turnover and differentiation remains less understood. Intestinal stem and progenitor cells are essential for the maintenance of intestinal homeostasis and regeneration, and their functions can be modulated by factors of the stem cell niche, including neuronal mediators. Here, we investigated the role of VIP in regulating intestinal epithelial homeostasis and regeneration following irradiation-induced injury.BACKGROUNDVasoactive intestinal peptide (VIP) is a neuronal peptide with prominent distribution along the enteric nervous system. While effects of VIP on intestinal motility, mucosal vasodilation, secretion, and mucosal immune cell function are well-studied, the direct impact of VIP on intestinal epithelial cell turnover and differentiation remains less understood. Intestinal stem and progenitor cells are essential for the maintenance of intestinal homeostasis and regeneration, and their functions can be modulated by factors of the stem cell niche, including neuronal mediators. Here, we investigated the role of VIP in regulating intestinal epithelial homeostasis and regeneration following irradiation-induced injury.Jejunal organoids were derived from male and female C57Bl6/J, Lgr5-EGFP-IRES-CreERT2 or Lgr5-EGFP-IRES-CreERT2/R26R-LSL-TdTomato mice and treated with VIP prior to analysis. Injury conditions were induced by exposing organoids to 6 Gy of irradiation (IR). To investigate protective effects of VIP in vivo, mice received 12 Gy of abdominal IR followed by intraperitoneal injections of VIP.METHODSJejunal organoids were derived from male and female C57Bl6/J, Lgr5-EGFP-IRES-CreERT2 or Lgr5-EGFP-IRES-CreERT2/R26R-LSL-TdTomato mice and treated with VIP prior to analysis. Injury conditions were induced by exposing organoids to 6 Gy of irradiation (IR). To investigate protective effects of VIP in vivo, mice received 12 Gy of abdominal IR followed by intraperitoneal injections of VIP.We observed that VIP promotes epithelial differentiation towards a secretory phenotype predominantly via the p38 MAPK pathway. Moreover, VIP prominently modulated epithelial proliferation as well as the number and proliferative activity of Lgr5-EGFP+ progenitor cells under homeostatic conditions. In the context of acute irradiation injury in vitro, we observed that IR injury renders Lgr5-EGFP+ progenitor cells more susceptible to VIP-induced modulations, which coincided with the strong promotion of epithelial regeneration by VIP. Finally, the observed effects translate into an in vivo model of abdominal irradiation, where VIP showed to prominently mitigate radiation-induced injury.RESULTSWe observed that VIP promotes epithelial differentiation towards a secretory phenotype predominantly via the p38 MAPK pathway. Moreover, VIP prominently modulated epithelial proliferation as well as the number and proliferative activity of Lgr5-EGFP+ progenitor cells under homeostatic conditions. In the context of acute irradiation injury in vitro, we observed that IR injury renders Lgr5-EGFP+ progenitor cells more susceptible to VIP-induced modulations, which coincided with the strong promotion of epithelial regeneration by VIP. Finally, the observed effects translate into an in vivo model of abdominal irradiation, where VIP showed to prominently mitigate radiation-induced injury.VIP prominently governs intestinal homeostasis by regulating epithelial progenitor cell proliferation and differentiation and promotes intestinal regeneration following acute irradiation injury.CONCLUSIONSVIP prominently governs intestinal homeostasis by regulating epithelial progenitor cell proliferation and differentiation and promotes intestinal regeneration following acute irradiation injury. Vasoactive intestinal peptide (VIP) is a neuronal peptide with prominent distribution along the enteric nervous system. While effects of VIP on intestinal motility, mucosal vasodilation, secretion, and mucosal immune cell function are well-studied, the direct impact of VIP on intestinal epithelial cell turnover and differentiation remains less understood. Intestinal stem and progenitor cells are essential for the maintenance of intestinal homeostasis and regeneration, and their functions can be modulated by factors of the stem cell niche, including neuronal mediators. Here, we investigated the role of VIP in regulating intestinal epithelial homeostasis and regeneration following irradiation-induced injury. Jejunal organoids were derived from male and female C57Bl6/J, Lgr5-EGFP-IRES-CreER.sup.T2 or Lgr5-EGFP-IRES-CreER.sup.T2/R26R-LSL-TdTomato mice and treated with VIP prior to analysis. Injury conditions were induced by exposing organoids to 6 Gy of irradiation (IR). To investigate protective effects of VIP in vivo, mice received 12 Gy of abdominal IR followed by intraperitoneal injections of VIP. We observed that VIP promotes epithelial differentiation towards a secretory phenotype predominantly via the p38 MAPK pathway. Moreover, VIP prominently modulated epithelial proliferation as well as the number and proliferative activity of Lgr5-EGFP.sup.+ progenitor cells under homeostatic conditions. In the context of acute irradiation injury in vitro, we observed that IR injury renders Lgr5-EGFP.sup.+ progenitor cells more susceptible to VIP-induced modulations, which coincided with the strong promotion of epithelial regeneration by VIP. Finally, the observed effects translate into an in vivo model of abdominal irradiation, where VIP showed to prominently mitigate radiation-induced injury. VIP prominently governs intestinal homeostasis by regulating epithelial progenitor cell proliferation and differentiation and promotes intestinal regeneration following acute irradiation injury. Vasoactive intestinal peptide (VIP) is a neuronal peptide with prominent distribution along the enteric nervous system. While effects of VIP on intestinal motility, mucosal vasodilation, secretion, and mucosal immune cell function are well-studied, the direct impact of VIP on intestinal epithelial cell turnover and differentiation remains less understood. Intestinal stem and progenitor cells are essential for the maintenance of intestinal homeostasis and regeneration, and their functions can be modulated by factors of the stem cell niche, including neuronal mediators. Here, we investigated the role of VIP in regulating intestinal epithelial homeostasis and regeneration following irradiation-induced injury. Jejunal organoids were derived from male and female C57Bl6/J, Lgr5-EGFP-IRES-CreER or Lgr5-EGFP-IRES-CreER /R26R-LSL-TdTomato mice and treated with VIP prior to analysis. Injury conditions were induced by exposing organoids to 6 Gy of irradiation (IR). To investigate protective effects of VIP in vivo, mice received 12 Gy of abdominal IR followed by intraperitoneal injections of VIP. We observed that VIP promotes epithelial differentiation towards a secretory phenotype predominantly via the p38 MAPK pathway. Moreover, VIP prominently modulated epithelial proliferation as well as the number and proliferative activity of Lgr5-EGFP progenitor cells under homeostatic conditions. In the context of acute irradiation injury in vitro, we observed that IR injury renders Lgr5-EGFP progenitor cells more susceptible to VIP-induced modulations, which coincided with the strong promotion of epithelial regeneration by VIP. Finally, the observed effects translate into an in vivo model of abdominal irradiation, where VIP showed to prominently mitigate radiation-induced injury. VIP prominently governs intestinal homeostasis by regulating epithelial progenitor cell proliferation and differentiation and promotes intestinal regeneration following acute irradiation injury. |
| ArticleNumber | 348 |
| Audience | Academic |
| Author | Ragab, Mohab Ermolova, Anastasia Giller, Maximilian Waldherr Ávila de Melo, Caroline Saur, Dieter Quante, Michael Steiger, Katja Schmid, Roland M. Wieland, Jessica Kohnke-Ertel, Birgit Maurer, H. Carlo Öllinger, Rupert Middelhoff, Moritz Demir, Ihsan Ekin Fischer, Julius Clemens Agibalova, Tatiana Heindl, Fabian Tschurtschenthaler, Markus Hempel, Anneke |
| Author_xml | – sequence: 1 givenname: Tatiana surname: Agibalova fullname: Agibalova, Tatiana organization: Department of Internal Medicine II, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich – sequence: 2 givenname: Anneke surname: Hempel fullname: Hempel, Anneke organization: Department of Internal Medicine II, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich – sequence: 3 givenname: H. Carlo surname: Maurer fullname: Maurer, H. Carlo organization: Department of Internal Medicine II, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich – sequence: 4 givenname: Mohab surname: Ragab fullname: Ragab, Mohab organization: Department of Internal Medicine II, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich – sequence: 5 givenname: Anastasia surname: Ermolova fullname: Ermolova, Anastasia organization: Department of Internal Medicine II, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich – sequence: 6 givenname: Jessica surname: Wieland fullname: Wieland, Jessica organization: Department of Internal Medicine II, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich – sequence: 7 givenname: Caroline surname: Waldherr Ávila de Melo fullname: Waldherr Ávila de Melo, Caroline organization: Department of Internal Medicine II, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich – sequence: 8 givenname: Fabian surname: Heindl fullname: Heindl, Fabian organization: Department of Internal Medicine II, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich – sequence: 9 givenname: Maximilian surname: Giller fullname: Giller, Maximilian organization: Department of Radiation Oncology, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich – sequence: 10 givenname: Julius Clemens surname: Fischer fullname: Fischer, Julius Clemens organization: Department of Radiation Oncology, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich – sequence: 11 givenname: Markus surname: Tschurtschenthaler fullname: Tschurtschenthaler, Markus organization: Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Chair of Translational Cancer Research and Institute of Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine and Health, Technical University of Munich, Center for Translational Cancer Research (TranslaTUM), Klinikum rechts der Isar, School of Medicine and Health, Technical University of Munich – sequence: 12 givenname: Birgit surname: Kohnke-Ertel fullname: Kohnke-Ertel, Birgit organization: Department of Internal Medicine II, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich – sequence: 13 givenname: Rupert surname: Öllinger fullname: Öllinger, Rupert organization: Institute of Molecular Oncology and Functional Genomics, Center for Translational Cancer Research (TranslaTUM), TUM School of Medicine and Health, Technical University of Munich – sequence: 14 givenname: Katja surname: Steiger fullname: Steiger, Katja organization: Institute of Pathology, TUM School of Medicine and Health, Technical University of Munich – sequence: 15 givenname: Ihsan Ekin surname: Demir fullname: Demir, Ihsan Ekin organization: Department of Surgery, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich, Else Kröner Clinician Scientist Professor for Translational Pancreatic Surgery – sequence: 16 givenname: Dieter surname: Saur fullname: Saur, Dieter organization: Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Chair of Translational Cancer Research and Institute of Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine and Health, Technical University of Munich, Center for Translational Cancer Research (TranslaTUM), Klinikum rechts der Isar, School of Medicine and Health, Technical University of Munich – sequence: 17 givenname: Michael surname: Quante fullname: Quante, Michael organization: Department of Internal Medicine II, Faculty of Medicine, Freiburg University Medical Center, University of Freiburg – sequence: 18 givenname: Roland M. surname: Schmid fullname: Schmid, Roland M. organization: Department of Internal Medicine II, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich – sequence: 19 givenname: Moritz orcidid: 0000-0001-8425-3985 surname: Middelhoff fullname: Middelhoff, Moritz email: moritz.middelhoff@mri.tum.de organization: Department of Internal Medicine II, Klinikum rechts der Isar, TUM School of Medicine and Health, Technical University of Munich |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/39380035$$D View this record in MEDLINE/PubMed |
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| Keywords | Irradiation Regeneration Intestinal progenitor cells VIP |
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Vasoactive intestinal peptide (VIP) is a neuronal peptide with prominent distribution along the enteric nervous system. While effects of VIP on... Vasoactive intestinal peptide (VIP) is a neuronal peptide with prominent distribution along the enteric nervous system. While effects of VIP on intestinal... Background Vasoactive intestinal peptide (VIP) is a neuronal peptide with prominent distribution along the enteric nervous system. While effects of VIP on... Abstract Background Vasoactive intestinal peptide (VIP) is a neuronal peptide with prominent distribution along the enteric nervous system. While effects of... |
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| SubjectTerms | Animals Biomedical and Life Sciences Biomedical Engineering and Bioengineering Blood vessels Cell Biology Cell Differentiation Dilatation Ethylenediaminetetraacetic acid Female Flumazenil Intestinal Mucosa - metabolism Intestinal Mucosa - pathology Intestinal Mucosa - radiation effects Intestinal progenitor cells Irradiation Life Sciences Male Mice Mice, Inbred C57BL Organoids - metabolism Radiation Radiation Injuries - metabolism Radiation Injuries - pathology Regeneration Regenerative Medicine/Tissue Engineering Scientific equipment and supplies industry Stem Cells Stem Cells - drug effects Stem Cells - metabolism Stem Cells - radiation effects Vasoactive Intestinal Peptide - metabolism Vasoactive Intestinal Peptide - pharmacology Vasoactive intestinal peptides VIP |
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| Title | Vasoactive intestinal peptide promotes secretory differentiation and mitigates radiation-induced intestinal injury |
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