Identification of liver‐derived bone morphogenetic protein (BMP)‐9 as a potential new candidate for treatment of colorectal cancer
Colorectal cancer (CRC) is a high‐incidence malignancy worldwide which still needs better therapy options. Therefore, the aim of the present study was to investigate the responses of normal or malignant human intestinal epithelium to bone morphogenetic protein (BMP)‐9 and to find out whether the app...
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| Published in | Journal of cellular and molecular medicine Vol. 26; no. 2; pp. 343 - 353 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
John Wiley & Sons, Inc
01.01.2022
John Wiley and Sons Inc |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1582-1838 1582-4934 1582-4934 |
| DOI | 10.1111/jcmm.17084 |
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| Abstract | Colorectal cancer (CRC) is a high‐incidence malignancy worldwide which still needs better therapy options. Therefore, the aim of the present study was to investigate the responses of normal or malignant human intestinal epithelium to bone morphogenetic protein (BMP)‐9 and to find out whether the application of BMP‐9 to patients with CRC or the enhancement of its synthesis in the liver could be useful strategies for new therapy approaches. In silico analyses of CRC patient cohorts (TCGA database) revealed that high expression of the BMP‐target gene ID1, especially in combination with low expression of the BMP‐inhibitor noggin, is significantly associated with better patient survival. Organoid lines were generated from human biopsies of colon cancer (T‐Orgs) and corresponding non‐malignant areas (N‐Orgs) of three patients. The N‐Orgs represented tumours belonging to three different consensus molecular subtypes (CMS) of CRC. Overall, BMP‐9 stimulation of organoids promoted an enrichment of tumour‐suppressive gene expression signatures, whereas the stimulation with noggin had the opposite effects. Furthermore, treatment of organoids with BMP‐9 induced ID1 expression (independently of high noggin levels), while treatment with noggin reduced ID1.
In summary, our data identify the ratio between ID1 and noggin as a new prognostic value for CRC patient outcome. We further show that by inducing ID1, BMP‐9 enhances this ratio, even in the presence of noggin. Thus, BMP‐9 is identified as a novel target for the development of improved anti‐cancer therapies of patients with CRC. |
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| AbstractList | Colorectal cancer (CRC) is a high-incidence malignancy worldwide which still needs better therapy options. Therefore, the aim of the present study was to investigate the responses of normal or malignant human intestinal epithelium to bone morphogenetic protein (BMP)-9 and to find out whether the application of BMP-9 to patients with CRC or the enhancement of its synthesis in the liver could be useful strategies for new therapy approaches. In silico analyses of CRC patient cohorts (TCGA database) revealed that high expression of the BMP-target gene ID1, especially in combination with low expression of the BMP-inhibitor noggin, is significantly associated with better patient survival. Organoid lines were generated from human biopsies of colon cancer (T-Orgs) and corresponding non-malignant areas (N-Orgs) of three patients. The N-Orgs represented tumours belonging to three different consensus molecular subtypes (CMS) of CRC. Overall, BMP-9 stimulation of organoids promoted an enrichment of tumour-suppressive gene expression signatures, whereas the stimulation with noggin had the opposite effects. Furthermore, treatment of organoids with BMP-9 induced ID1 expression (independently of high noggin levels), while treatment with noggin reduced ID1. In summary, our data identify the ratio between ID1 and noggin as a new prognostic value for CRC patient outcome. We further show that by inducing ID1, BMP-9 enhances this ratio, even in the presence of noggin. Thus, BMP-9 is identified as a novel target for the development of improved anti-cancer therapies of patients with CRC. Colorectal cancer (CRC) is a high‐incidence malignancy worldwide which still needs better therapy options. Therefore, the aim of the present study was to investigate the responses of normal or malignant human intestinal epithelium to bone morphogenetic protein (BMP)‐9 and to find out whether the application of BMP‐9 to patients with CRC or the enhancement of its synthesis in the liver could be useful strategies for new therapy approaches. In silico analyses of CRC patient cohorts (TCGA database) revealed that high expression of the BMP‐target gene ID1, especially in combination with low expression of the BMP‐inhibitor noggin, is significantly associated with better patient survival. Organoid lines were generated from human biopsies of colon cancer (T‐Orgs) and corresponding non‐malignant areas (N‐Orgs) of three patients. The N‐Orgs represented tumours belonging to three different consensus molecular subtypes (CMS) of CRC. Overall, BMP‐9 stimulation of organoids promoted an enrichment of tumour‐suppressive gene expression signatures, whereas the stimulation with noggin had the opposite effects. Furthermore, treatment of organoids with BMP‐9 induced ID1 expression (independently of high noggin levels), while treatment with noggin reduced ID1. In summary, our data identify the ratio between ID1 and noggin as a new prognostic value for CRC patient outcome. We further show that by inducing ID1, BMP‐9 enhances this ratio, even in the presence of noggin. Thus, BMP‐9 is identified as a novel target for the development of improved anti‐cancer therapies of patients with CRC. Colorectal cancer (CRC) is a high-incidence malignancy worldwide which still needs better therapy options. Therefore, the aim of the present study was to investigate the responses of normal or malignant human intestinal epithelium to bone morphogenetic protein (BMP)-9 and to find out whether the application of BMP-9 to patients with CRC or the enhancement of its synthesis in the liver could be useful strategies for new therapy approaches. In silico analyses of CRC patient cohorts (TCGA database) revealed that high expression of the BMP-target gene ID1, especially in combination with low expression of the BMP-inhibitor noggin, is significantly associated with better patient survival. Organoid lines were generated from human biopsies of colon cancer (T-Orgs) and corresponding non-malignant areas (N-Orgs) of three patients. The N-Orgs represented tumours belonging to three different consensus molecular subtypes (CMS) of CRC. Overall, BMP-9 stimulation of organoids promoted an enrichment of tumour-suppressive gene expression signatures, whereas the stimulation with noggin had the opposite effects. Furthermore, treatment of organoids with BMP-9 induced ID1 expression (independently of high noggin levels), while treatment with noggin reduced ID1. In summary, our data identify the ratio between ID1 and noggin as a new prognostic value for CRC patient outcome. We further show that by inducing ID1, BMP-9 enhances this ratio, even in the presence of noggin. Thus, BMP-9 is identified as a novel target for the development of improved anti-cancer therapies of patients with CRC.Colorectal cancer (CRC) is a high-incidence malignancy worldwide which still needs better therapy options. Therefore, the aim of the present study was to investigate the responses of normal or malignant human intestinal epithelium to bone morphogenetic protein (BMP)-9 and to find out whether the application of BMP-9 to patients with CRC or the enhancement of its synthesis in the liver could be useful strategies for new therapy approaches. In silico analyses of CRC patient cohorts (TCGA database) revealed that high expression of the BMP-target gene ID1, especially in combination with low expression of the BMP-inhibitor noggin, is significantly associated with better patient survival. Organoid lines were generated from human biopsies of colon cancer (T-Orgs) and corresponding non-malignant areas (N-Orgs) of three patients. The N-Orgs represented tumours belonging to three different consensus molecular subtypes (CMS) of CRC. Overall, BMP-9 stimulation of organoids promoted an enrichment of tumour-suppressive gene expression signatures, whereas the stimulation with noggin had the opposite effects. Furthermore, treatment of organoids with BMP-9 induced ID1 expression (independently of high noggin levels), while treatment with noggin reduced ID1. In summary, our data identify the ratio between ID1 and noggin as a new prognostic value for CRC patient outcome. We further show that by inducing ID1, BMP-9 enhances this ratio, even in the presence of noggin. Thus, BMP-9 is identified as a novel target for the development of improved anti-cancer therapies of patients with CRC. Colorectal cancer (CRC) is a high‐incidence malignancy worldwide which still needs better therapy options. Therefore, the aim of the present study was to investigate the responses of normal or malignant human intestinal epithelium to bone morphogenetic protein (BMP)‐9 and to find out whether the application of BMP‐9 to patients with CRC or the enhancement of its synthesis in the liver could be useful strategies for new therapy approaches. In silico analyses of CRC patient cohorts (TCGA database) revealed that high expression of the BMP‐target gene ID1, especially in combination with low expression of the BMP‐inhibitor noggin, is significantly associated with better patient survival. Organoid lines were generated from human biopsies of colon cancer (T‐Orgs) and corresponding non‐malignant areas (N‐Orgs) of three patients. The N‐Orgs represented tumours belonging to three different consensus molecular subtypes (CMS) of CRC. Overall, BMP‐9 stimulation of organoids promoted an enrichment of tumour‐suppressive gene expression signatures, whereas the stimulation with noggin had the opposite effects. Furthermore, treatment of organoids with BMP‐9 induced ID1 expression (independently of high noggin levels), while treatment with noggin reduced ID1.In summary, our data identify the ratio between ID1 and noggin as a new prognostic value for CRC patient outcome. We further show that by inducing ID1, BMP‐9 enhances this ratio, even in the presence of noggin. Thus, BMP‐9 is identified as a novel target for the development of improved anti‐cancer therapies of patients with CRC. |
| Author | Betge, Johannes Torre, Carolina Gretz, Norbert Rahbari, Nuh N. Itzel, Timo Ebert, Matthias P. Teufel, Andreas Breitkopf‐Heinlein, Katja Cai, Chen Gaitantzi, Haristi Birgin, Emrullah |
| AuthorAffiliation | 2 Medical Research Center University Medical Center Mannheim Medical Faculty Mannheim Heidelberg University Mannheim Germany 3 Department of Surgery University Medical Center Mannheim Medical Faculty Mannheim Heidelberg University Mannheim Germany 1 Department of Medicine II University Medical Center Mannheim Medical Faculty Mannheim Heidelberg University Mannheim Germany |
| AuthorAffiliation_xml | – name: 1 Department of Medicine II University Medical Center Mannheim Medical Faculty Mannheim Heidelberg University Mannheim Germany – name: 2 Medical Research Center University Medical Center Mannheim Medical Faculty Mannheim Heidelberg University Mannheim Germany – name: 3 Department of Surgery University Medical Center Mannheim Medical Faculty Mannheim Heidelberg University Mannheim Germany |
| Author_xml | – sequence: 1 givenname: Chen orcidid: 0000-0001-6226-3269 surname: Cai fullname: Cai, Chen organization: Heidelberg University – sequence: 2 givenname: Timo surname: Itzel fullname: Itzel, Timo organization: Heidelberg University – sequence: 3 givenname: Haristi surname: Gaitantzi fullname: Gaitantzi, Haristi organization: Heidelberg University – sequence: 4 givenname: Carolina surname: Torre fullname: Torre, Carolina organization: Heidelberg University – sequence: 5 givenname: Emrullah surname: Birgin fullname: Birgin, Emrullah organization: Heidelberg University – sequence: 6 givenname: Johannes surname: Betge fullname: Betge, Johannes organization: Heidelberg University – sequence: 7 givenname: Norbert surname: Gretz fullname: Gretz, Norbert organization: Heidelberg University – sequence: 8 givenname: Andreas surname: Teufel fullname: Teufel, Andreas organization: Heidelberg University – sequence: 9 givenname: Nuh N. surname: Rahbari fullname: Rahbari, Nuh N. organization: Heidelberg University – sequence: 10 givenname: Matthias P. surname: Ebert fullname: Ebert, Matthias P. organization: Heidelberg University – sequence: 11 givenname: Katja orcidid: 0000-0002-1814-4796 surname: Breitkopf‐Heinlein fullname: Breitkopf‐Heinlein, Katja email: katja.breitkopf@medma.uni-heidelberg.de organization: Heidelberg University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34841646$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1016_j_livres_2024_09_006 crossref_primary_10_1016_j_mce_2023_111934 |
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| Copyright | 2021 The Authors. published by Foundation for Cellular and Molecular Medicine and John Wiley & Sons Ltd. 2021 The Authors. Journal of Cellular and Molecular Medicine published by Foundation for Cellular and Molecular Medicine and John Wiley & Sons Ltd. 2022. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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| Keywords | colorectal cancer bone morphogenetic protein-9 ID1 noggin |
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| License | Attribution 2021 The Authors. Journal of Cellular and Molecular Medicine published by Foundation for Cellular and Molecular Medicine and John Wiley & Sons Ltd. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
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| Notes | K.B.H. and H.G. were supported by funding from the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) (Project No.: 393225014; 394046768‐SFB1366). C.C. was a fellow supported by the China Scholarship Council (CSC) and by Integrated Hospital of traditional Chinese Medicine, Southern Medical University. Funding Information ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 |
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| Snippet | Colorectal cancer (CRC) is a high‐incidence malignancy worldwide which still needs better therapy options. Therefore, the aim of the present study was to... Colorectal cancer (CRC) is a high-incidence malignancy worldwide which still needs better therapy options. Therefore, the aim of the present study was to... |
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| SubjectTerms | Biopsy Bone Morphogenetic Protein 2 Bone Morphogenetic Protein 4 - pharmacology Bone morphogenetic proteins Bone Morphogenetic Proteins - genetics Bone Morphogenetic Proteins - metabolism bone morphogenetic protein‐9 Cancer therapies Colon cancer Colonic Neoplasms Colorectal cancer Colorectal carcinoma Colorectal Neoplasms - genetics Epithelium Gene expression Genes Growth Differentiation Factor 2 - genetics Homeostasis Humans ID1 Id1 protein Inhibitor of Differentiation Protein 1 Liver Liver - metabolism Malignancy Metastasis noggin Noggin protein Organoids Original Patients Proteins Signal Transduction Tumors |
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| Title | Identification of liver‐derived bone morphogenetic protein (BMP)‐9 as a potential new candidate for treatment of colorectal cancer |
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