Notch1 functions as a tumor suppressor in mouse skin
Notch proteins are important in binary cell-fate decisions and inhibiting differentiation in many developmental systems, and aberrant Notch signaling is associated with tumorigenesis. The role of Notch signaling in mammalian skin is less well characterized and is mainly based on in vitro studies, wh...
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| Published in | Nature genetics Vol. 33; no. 3; pp. 416 - 421 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.03.2003
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Notch proteins are important in binary cell-fate decisions and inhibiting differentiation in many developmental systems, and aberrant Notch signaling is associated with tumorigenesis. The role of Notch signaling in mammalian skin is less well characterized and is mainly based on in vitro studies, which suggest that Notch signaling induces differentiation in mammalian skin. Conventional gene targeting is not applicable to establishing the role of Notch receptors or ligands in the skin because Notch1−/− embryos die during gestation. Therefore, we used a tissue-specific inducible gene-targeting approach to study the physiological role of the Notch1 receptor in the mouse epidermis and the corneal epithelium of adult mice. Unexpectedly, ablation of Notch1 results in epidermal and corneal hyperplasia followed by the development of skin tumors and facilitated chemical-induced skin carcinogenesis. Notch1 deficiency in skin and in primary keratinocytes results in increased and sustained expression of Gli2, causing the development of basal-cell carcinoma-like tumors. Furthermore, Notch1 inactivation in the epidermis results in derepressed β-catenin signaling in cells that should normally undergo differentiation. Enhanced β-catenin signaling can be reversed by re-introduction of a dominant active form of the Notch1 receptor. This leads to a reduction in the signaling-competent pool of β-catenin, indicating that Notch1 can inhibit β-catenin-mediated signaling. Our results indicate that Notch1 functions as a tumor-suppressor gene in mammalian skin. |
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| AbstractList | Notch proteins are important in binary cell-fate decisions and inhibiting differentiation in many developmental systems, and aberrant Notch signaling is associated with tumorigenesis. The role of Notch signaling in mammalian skin is less well characterized and is mainly based on in vitro studies, which suggest that Notch signaling induces differentiation in mammalian skin. Conventional gene targeting is not applicable to establishing the role of Notch receptors or ligands in the skin because Notch1 super(-/-) embryos die during gestation. Therefore, we used a tissue-specific inducible gene-targeting approach to study the physiological role of the Notch1 receptor in the mouse epidermis and the corneal epithelium of adult mice. Unexpectedly, ablation of Notch1 results in epidermal and corneal hyperplasia followed by the development of skin tumors and facilitated chemical-induced skin carcinogenesis. Notch1 deficiency in skin and in primary keratinocytes results in increased and sustained expression of Gli2, causing the development of basal-cell carcinoma-like tumors. Furthermore, Notch1 inactivation in the epidermis results in derepressed beta -catenin signaling in cells that should normally undergo differentiation. Enhanced beta -catenin signaling can be reversed by re-introduction of a dominant active form of the Notch1 receptor. This leads to a reduction in the signaling-competent pool of beta -catenin, indicating that Notch1 can inhibit beta -catenin-mediated signaling. Our results indicate that Notch1 functions as a tumor-suppressor gene in mammalian skin. Notch proteins are important in binary cell-fate decisions and inhibiting differentiation in many developmental systems, and aberrant Notch signaling is associated with tumorigenesis. The role of Notch signaling in mammalian skin is less well characterized and is mainly based on in vitro studies, which suggest that Notch signaling induces differentiation in mammalian skin. Conventional gene targeting is not applicable to establishing the role of Notch receptors or ligands in the skin because Notch1−/− embryos die during gestation. Therefore, we used a tissue-specific inducible gene-targeting approach to study the physiological role of the Notch1 receptor in the mouse epidermis and the corneal epithelium of adult mice. Unexpectedly, ablation of Notch1 results in epidermal and corneal hyperplasia followed by the development of skin tumors and facilitated chemical-induced skin carcinogenesis. Notch1 deficiency in skin and in primary keratinocytes results in increased and sustained expression of Gli2, causing the development of basal-cell carcinoma-like tumors. Furthermore, Notch1 inactivation in the epidermis results in derepressed β-catenin signaling in cells that should normally undergo differentiation. Enhanced β-catenin signaling can be reversed by re-introduction of a dominant active form of the Notch1 receptor. This leads to a reduction in the signaling-competent pool of β-catenin, indicating that Notch1 can inhibit β-catenin-mediated signaling. Our results indicate that Notch1 functions as a tumor-suppressor gene in mammalian skin. Notch proteins are important in binary cell-fate decisions and inhibiting differentiation in many developmental systems, and aberrant Notch signaling is associated with tumorigenesis. The role of Notch signaling in mammalian skin is less well characterized and is mainly based on in vitro studies, which suggest that Notch signaling induces differentiation in mammalian skin. Conventional gene targeting is not applicable to establishing the role of Notch receptors or ligands in the skin because Notch1-/- embryos die during gestation. Therefore, we used a tissue-specific inducible gene-targeting approach to study the physiological role of the Notch1 receptor in the mouse epidermis and the corneal epithelium of adult mice. Unexpectedly, ablation of Notch1 results in epidermal and corneal hyperplasia followed by the development of skin tumors and facilitated chemical-induced skin carcinogenesis. Notch1 deficiency in skin and in primary keratinocytes results in increased and sustained expression of Gli2, causing the development of basal-cell carcinoma-like tumors. Furthermore, Notch1 inactivation in the epidermis results in derepressed beta-catenin signaling in cells that should normally undergo differentiation. Enhanced beta-catenin signaling can be reversed by re-introduction of a dominant active form of the Notch1 receptor. This leads to a reduction in the signaling-competent pool of beta-catenin, indicating that Notch1 can inhibit beta-catenin-mediated signaling. Our results indicate that Notch1 functions as a tumor-suppressor gene in mammalian skin. Notch proteins are important in binary cell-fate decisions and inhibiting differentiation in many developmental systems 1 , and aberrant Notch signaling is associated with tumorigenesis 2 , 3 , 4 , 5 . The role of Notch signaling in mammalian skin is less well characterized and is mainly based on in vitro studies, which suggest that Notch signaling induces differentiation in mammalian skin 6 , 7 . Conventional gene targeting is not applicable to establishing the role of Notch receptors or ligands in the skin because Notch1 −/− embryos die during gestation 8 , 9 , 10 , 11 , 12 . Therefore, we used a tissue-specific inducible gene-targeting approach to study the physiological role of the Notch1 receptor in the mouse epidermis and the corneal epithelium of adult mice. Unexpectedly, ablation of Notch1 results in epidermal and corneal hyperplasia followed by the development of skin tumors and facilitated chemical-induced skin carcinogenesis. Notch1 deficiency in skin and in primary keratinocytes results in increased and sustained expression of Gli2 , causing the development of basal-cell carcinoma–like tumors. Furthermore, Notch1 inactivation in the epidermis results in derepressed β-catenin signaling in cells that should normally undergo differentiation. Enhanced β-catenin signaling can be reversed by re-introduction of a dominant active form of the Notch1 receptor. This leads to a reduction in the signaling-competent pool of β-catenin, indicating that Notch1 can inhibit β-catenin-mediated signaling. Our results indicate that Notch1 functions as a tumor-suppressor gene in mammalian skin. |
| Audience | Academic |
| Author | Wolfer, Anita Clevers, Hans Kummer, J. Alain Radtke, Freddy van Noort, Mascha Mill, Pleasantine Nicolas, Michael Dotto, G. Paolo Hui, Chi-chung Raj, Kenneth |
| Author_xml | – givenname: Anita surname: Wolfer fullname: Wolfer, Anita organization: Ludwig Institute for Cancer Research, Lausanne Branch, University Lausanne – givenname: Freddy surname: Radtke fullname: Radtke, Freddy organization: Ludwig Institute for Cancer Research, Lausanne Branch, University Lausanne – givenname: Michael surname: Nicolas fullname: Nicolas, Michael organization: Ludwig Institute for Cancer Research, Lausanne Branch, University Lausanne Swiss Institute for Experimental Cancer Research – givenname: G. Paolo surname: Dotto fullname: Dotto, G. Paolo organization: Cutaneous Biology Research Center, Massachusetts General Hospital and Harvard Medical School – givenname: J. Alain surname: Kummer fullname: Kummer, J. Alain organization: Department of Pathology, VU University Medical Center – givenname: Pleasantine surname: Mill fullname: Mill, Pleasantine organization: Program in Developmental Biology, The Hospital for Sick Children and Department of Molecular and Medical Genetics, University of Toronto – givenname: Hans surname: Clevers fullname: Clevers, Hans organization: Department of Immunology, Erasmus University Rotterdam/University 3000 DR Rotterdam and Departments of Immunology and Cell Biology, University Medical Center Utrecht – givenname: Mascha surname: van Noort fullname: van Noort, Mascha organization: Department of Immunology, Erasmus University Rotterdam/University 3000 DR Rotterdam and Departments of Immunology and Cell Biology, University Medical Center Utrecht – givenname: Chi-chung surname: Hui fullname: Hui, Chi-chung organization: Program in Developmental Biology, The Hospital for Sick Children and Department of Molecular and Medical Genetics, University of Toronto – givenname: Kenneth surname: Raj fullname: Raj, Kenneth organization: Swiss Institute for Experimental Cancer Research |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=14690670$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/12590261$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Springer Nature America, Inc. 2003 2003 INIST-CNRS COPYRIGHT 2003 Nature Publishing Group Copyright Nature Publishing Group Mar 2003 |
| Copyright_xml | – notice: Springer Nature America, Inc. 2003 – notice: 2003 INIST-CNRS – notice: COPYRIGHT 2003 Nature Publishing Group – notice: Copyright Nature Publishing Group Mar 2003 |
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| DOI | 10.1038/ng1099 |
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| Keywords | Vertebrata Mammalia Mouse Rodentia Suppressor Tumor Skin |
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| SubjectTerms | Agriculture Animal Genetics and Genomics Animals beta Catenin Biological and medical sciences Biomedical and Life Sciences Biomedicine Cancer cells Cancer Research Carcinogenesis Cellular signal transduction Classical genetics, quantitative genetics, hybrids Cytoskeletal Proteins - metabolism DNA-Binding Proteins - metabolism Embryos Epidermis Fundamental and applied biological sciences. Psychology Gene Function Genes, Tumor Suppressor Genetic aspects Genetics of eukaryotes. Biological and molecular evolution Human Genetics Inactivation Keratinocytes - transplantation Kruppel-Like Transcription Factors letter Lymphoid Enhancer-Binding Factor 1 Mammals Membrane Proteins - deficiency Membrane Proteins - genetics Membrane Proteins - physiology Mice Mice, Knockout Mice, Nude Mice, Transgenic Physiological aspects Physiology Receptor, Notch1 Receptors, Cell Surface RNA, Messenger - genetics RNA, Messenger - metabolism Signal Transduction Skin Skin - metabolism Skin - pathology Skin Neoplasms - genetics Skin Neoplasms - pathology Skin Neoplasms - prevention & control Trans-Activators - metabolism Transcription Factors - genetics Transcription Factors - metabolism Tumor suppressor genes Tumors Vertebrata Zinc Finger Protein Gli2 |
| Title | Notch1 functions as a tumor suppressor in mouse skin |
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