Novel action of FOXL2 as mediator of Col1a2 gene autoregulation
FOXL2 belongs to the evolutionarily conserved forkhead box (FOX) superfamily and is a master transcription factor in a spectrum of developmental pathways, including ovarian and eyelid development and bone, cartilage and uterine maturation. To analyse its action, we searched for proteins that interac...
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| Published in: | Developmental biology Vol. 416; no. 1; pp. 200 - 211 |
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| Main Authors: | , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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01.08.2016
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| ISSN: | 0012-1606, 1095-564X, 1095-564X |
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| Abstract | FOXL2 belongs to the evolutionarily conserved forkhead box (FOX) superfamily and is a master transcription factor in a spectrum of developmental pathways, including ovarian and eyelid development and bone, cartilage and uterine maturation.
To analyse its action, we searched for proteins that interact with FOXL2. We found that FOXL2 interacts with specific C-terminal propeptides of several fibrillary collagens. Because these propeptides can participate in feedback regulation of collagen biosynthesis, we inferred that FOXL2 could thereby affect the transcription of the cognate collagen genes. Focusing on COL1A2, we found that FOXL2 indeed affects collagen synthesis, by binding to a DNA response element located about 65Kb upstream of this gene. According to our hypothesis we found that in Foxl2−/− mouse ovaries, Col1a2 was elevated from birth to adulthood.
The extracellular matrix (ECM) compartmentalizes the ovary during folliculogenesis, (with type I, type III and type IV collagens as primary components), and ECM composition changes during the reproductive lifespan. In Foxl2−/− mouse ovaries, in addition to up-regulation of Col1a2, Col3a1, Col4a1 and fibronectin were also upregulated, while laminin expression was reduced. Thus, by regulating levels of extracellular matrix components, FOXL2 may contribute to both ovarian histogenesis and the fibrosis attendant on depletion of the follicle reserve during reproductive aging and menopause.
•Forkhead transcription factor FOXL2 interacts with C-propeptides of COL1A2.•FOXL2 binds to a putative responsive element upstream of the Col1a2 gene.•FOXL2 binding to the target sequence activates a downstream Col1a2 promoter.•FOXL2 has a role in the dynamics of the ECM.•In Foxl2−/− mouse ovaries, Col1a2 is elevated from birth to adulthood. |
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| AbstractList | FOXL2 belongs to the evolutionarily conserved forkhead box (FOX) superfamily and is a master transcription factor in a spectrum of developmental pathways, including ovarian and eyelid development and bone, cartilage and uterine maturation. To analyse its action, we searched for proteins that interact with FOXL2. We found that FOXL2 interacts with specific C-terminal propeptides of several fibrillary collagens. Because these propeptides can participate in feedback regulation of collagen biosynthesis, we inferred that FOXL2 could thereby affect the transcription of the cognate collagen genes. Focusing on COL1A2, we found that FOXL2 indeed affects collagen synthesis, by binding to a DNA response element located about 65Kb upstream of this gene. According to our hypothesis we found that in Foxl2(-/-) mouse ovaries, Col1a2 was elevated from birth to adulthood. The extracellular matrix (ECM) compartmentalizes the ovary during folliculogenesis, (with type I, type III and type IV collagens as primary components), and ECM composition changes during the reproductive lifespan. In Foxl2(-/-) mouse ovaries, in addition to up-regulation of Col1a2, Col3a1, Col4a1 and fibronectin were also upregulated, while laminin expression was reduced. Thus, by regulating levels of extracellular matrix components, FOXL2 may contribute to both ovarian histogenesis and the fibrosis attendant on depletion of the follicle reserve during reproductive aging and menopause. FOXL2 belongs to the evolutionarily conserved forkhead box (FOX) superfamily and is a master transcription factor in a spectrum of developmental pathways, including ovarian and eyelid development and bone, cartilage and uterine maturation.To analyse its action, we searched for proteins that interact with FOXL2. We found that FOXL2 interacts with specific C-terminal propeptides of several fibrillary collagens. Because these propeptides can participate in feedback regulation of collagen biosynthesis, we inferred that FOXL2 could thereby affect the transcription of the cognate collagen genes. Focusing on COL1A2, we found that FOXL2 indeed affects collagen synthesis, by binding to a DNA response element located about 65Kb upstream of this gene. According to our hypothesis we found that in Foxl2−/− mouse ovaries, Col1a2 was elevated from birth to adulthood.The extracellular matrix (ECM) compartmentalizes the ovary during folliculogenesis, (with type I, type III and type IV collagens as primary components), and ECM composition changes during the reproductive lifespan. In Foxl2−/− mouse ovaries, in addition to up-regulation of Col1a2, Col3a1, Col4a1 and fibronectin were also upregulated, while laminin expression was reduced. Thus, by regulating levels of extracellular matrix components, FOXL2 may contribute to both ovarian histogenesis and the fibrosis attendant on depletion of the follicle reserve during reproductive aging and menopause. FOXL2 belongs to the evolutionarily conserved forkhead box (FOX) superfamily and is a master transcription factor in a spectrum of developmental pathways, including ovarian and eyelid development and bone, cartilage and uterine maturation. To analyse its action, we searched for proteins that interact with FOXL2. We found that FOXL2 interacts with specific C-terminal propeptides of several fibrillary collagens. Because these propeptides can participate in feedback regulation of collagen biosynthesis, we inferred that FOXL2 could thereby affect the transcription of the cognate collagen genes. Focusing on COL1A2, we found that FOXL2 indeed affects collagen synthesis, by binding to a DNA response element located about 65Kb upstream of this gene. According to our hypothesis we found that in Foxl2(-/-) mouse ovaries, Col1a2 was elevated from birth to adulthood. The extracellular matrix (ECM) compartmentalizes the ovary during folliculogenesis, (with type I, type III and type IV collagens as primary components), and ECM composition changes during the reproductive lifespan. In Foxl2(-/-) mouse ovaries, in addition to up-regulation of Col1a2, Col3a1, Col4a1 and fibronectin were also upregulated, while laminin expression was reduced. Thus, by regulating levels of extracellular matrix components, FOXL2 may contribute to both ovarian histogenesis and the fibrosis attendant on depletion of the follicle reserve during reproductive aging and menopause.FOXL2 belongs to the evolutionarily conserved forkhead box (FOX) superfamily and is a master transcription factor in a spectrum of developmental pathways, including ovarian and eyelid development and bone, cartilage and uterine maturation. To analyse its action, we searched for proteins that interact with FOXL2. We found that FOXL2 interacts with specific C-terminal propeptides of several fibrillary collagens. Because these propeptides can participate in feedback regulation of collagen biosynthesis, we inferred that FOXL2 could thereby affect the transcription of the cognate collagen genes. Focusing on COL1A2, we found that FOXL2 indeed affects collagen synthesis, by binding to a DNA response element located about 65Kb upstream of this gene. According to our hypothesis we found that in Foxl2(-/-) mouse ovaries, Col1a2 was elevated from birth to adulthood. The extracellular matrix (ECM) compartmentalizes the ovary during folliculogenesis, (with type I, type III and type IV collagens as primary components), and ECM composition changes during the reproductive lifespan. In Foxl2(-/-) mouse ovaries, in addition to up-regulation of Col1a2, Col3a1, Col4a1 and fibronectin were also upregulated, while laminin expression was reduced. Thus, by regulating levels of extracellular matrix components, FOXL2 may contribute to both ovarian histogenesis and the fibrosis attendant on depletion of the follicle reserve during reproductive aging and menopause. FOXL2 belongs to the evolutionarily conserved forkhead box (FOX) superfamily and is a master transcription factor in a spectrum of developmental pathways, including ovarian and eyelid development and bone, cartilage and uterine maturation. To analyse its action, we searched for proteins that interact with FOXL2. We found that FOXL2 interacts with specific C-terminal propeptides of several fibrillary collagens. Because these propeptides can participate in feedback regulation of collagen biosynthesis, we inferred that FOXL2 could thereby affect the transcription of the cognate collagen genes. Focusing on COL1A2, we found that FOXL2 indeed affects collagen synthesis, by binding to a DNA response element located about 65Kb upstream of this gene. According to our hypothesis we found that in Foxl2−/− mouse ovaries, Col1a2 was elevated from birth to adulthood. The extracellular matrix (ECM) compartmentalizes the ovary during folliculogenesis, (with type I, type III and type IV collagens as primary components), and ECM composition changes during the reproductive lifespan. In Foxl2−/− mouse ovaries, in addition to up-regulation of Col1a2, Col3a1, Col4a1 and fibronectin were also upregulated, while laminin expression was reduced. Thus, by regulating levels of extracellular matrix components, FOXL2 may contribute to both ovarian histogenesis and the fibrosis attendant on depletion of the follicle reserve during reproductive aging and menopause. •Forkhead transcription factor FOXL2 interacts with C-propeptides of COL1A2.•FOXL2 binds to a putative responsive element upstream of the Col1a2 gene.•FOXL2 binding to the target sequence activates a downstream Col1a2 promoter.•FOXL2 has a role in the dynamics of the ECM.•In Foxl2−/− mouse ovaries, Col1a2 is elevated from birth to adulthood. |
| Author | Marcia, Loredana Cusano, Roberto Deiana, Manila Cucca, Francesco Asunis, Isadora Marongiu, Mara Fotia, Giorgio Crisponi, Laura Loi, Angela Angius, Andrea Schlessinger, David Sbardellati, Andrea Meloni, Alessandra Crobu, Francesca |
| AuthorAffiliation | c Università degli Studi di Sassari, Sassari 07100, Italy b Centre for Advanced Studies, Research and Development in Sardinia (CRS4), Pula, Italy d Laboratory of Genetics, NIA-IRP, NIH, Baltimore, 21224-6825 MD, United States a Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato 09042, Italy |
| AuthorAffiliation_xml | – name: a Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato 09042, Italy – name: d Laboratory of Genetics, NIA-IRP, NIH, Baltimore, 21224-6825 MD, United States – name: c Università degli Studi di Sassari, Sassari 07100, Italy – name: b Centre for Advanced Studies, Research and Development in Sardinia (CRS4), Pula, Italy |
| Author_xml | – sequence: 1 givenname: Mara surname: Marongiu fullname: Marongiu, Mara organization: Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato 09042, Italy – sequence: 2 givenname: Manila surname: Deiana fullname: Deiana, Manila organization: Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato 09042, Italy – sequence: 3 givenname: Loredana surname: Marcia fullname: Marcia, Loredana organization: Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato 09042, Italy – sequence: 4 givenname: Andrea surname: Sbardellati fullname: Sbardellati, Andrea organization: Centre for Advanced Studies, Research and Development in Sardinia (CRS4), Pula, Italy – sequence: 5 givenname: Isadora surname: Asunis fullname: Asunis, Isadora organization: Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato 09042, Italy – sequence: 6 givenname: Alessandra surname: Meloni fullname: Meloni, Alessandra organization: Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato 09042, Italy – sequence: 7 givenname: Andrea surname: Angius fullname: Angius, Andrea organization: Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato 09042, Italy – sequence: 8 givenname: Roberto surname: Cusano fullname: Cusano, Roberto organization: Centre for Advanced Studies, Research and Development in Sardinia (CRS4), Pula, Italy – sequence: 9 givenname: Angela surname: Loi fullname: Loi, Angela organization: Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato 09042, Italy – sequence: 10 givenname: Francesca surname: Crobu fullname: Crobu, Francesca organization: Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato 09042, Italy – sequence: 11 givenname: Giorgio surname: Fotia fullname: Fotia, Giorgio organization: Centre for Advanced Studies, Research and Development in Sardinia (CRS4), Pula, Italy – sequence: 12 givenname: Francesco surname: Cucca fullname: Cucca, Francesco organization: Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato 09042, Italy – sequence: 13 givenname: David surname: Schlessinger fullname: Schlessinger, David organization: Laboratory of Genetics, NIA-IRP, NIH, Baltimore, 21224-6825 MD, United States – sequence: 14 givenname: Laura surname: Crisponi fullname: Crisponi, Laura email: laura.crisponi@irgb.cnr.it organization: Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato 09042, Italy |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27212026$$D View this record in MEDLINE/PubMed |
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| Keywords | Ovary FOXL2 COL1A2 Transcriptional regulation ECM |
| Language | English |
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| SubjectTerms | animal ovaries Animals autoregulation biosynthesis cartilage Cell Line Chromatin Immunoprecipitation COL1A2 collagen Collagen Type I - genetics Collagen Type I - metabolism Consensus Sequence DNA ECM extracellular matrix Extracellular Matrix - metabolism eyelids Female fibronectins fibrosis follicular development Forkhead Box Protein L2 Forkhead Transcription Factors - metabolism FOXL2 Gene Expression Regulation, Developmental genes laminin longevity menopause Mice Mice, Inbred C57BL morphogenesis Oligonucleotide Array Sequence Analysis Ovary Ovary - metabolism Promoter Regions, Genetic Protein Binding skeletal development transcription factors Transcriptional regulation |
| Title | Novel action of FOXL2 as mediator of Col1a2 gene autoregulation |
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