Quantitative single cell analysis of cell population dynamics during submandibular salivary gland development and differentiation
Summary Epithelial organ morphogenesis involves reciprocal interactions between epithelial and mesenchymal cell types to balance progenitor cell retention and expansion with cell differentiation for evolution of tissue architecture. Underlying submandibular salivary gland branching morphogenesis is...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
The Company of Biologists
2013-04-01
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| Series: | Biology Open |
| Subjects: | |
| Online Access: | http://bio.biologists.org/content/2/5/439 |
| _version_ | 1819138942266507264 |
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| author | Deirdre A. Nelson Charles Manhardt Vidya Kamath Yunxia Sui Alberto Santamaria-Pang Ali Can Musodiq Bello Alex Corwin Sean R. Dinn Michael Lazare Elise M. Gervais Sharon J. Sequeira Sarah B. Peters Fiona Ginty Michael J. Gerdes Melinda Larsen |
| author_facet | Deirdre A. Nelson Charles Manhardt Vidya Kamath Yunxia Sui Alberto Santamaria-Pang Ali Can Musodiq Bello Alex Corwin Sean R. Dinn Michael Lazare Elise M. Gervais Sharon J. Sequeira Sarah B. Peters Fiona Ginty Michael J. Gerdes Melinda Larsen |
| author_sort | Deirdre A. Nelson |
| collection | DOAJ |
| description | Summary
Epithelial organ morphogenesis involves reciprocal interactions between epithelial and mesenchymal cell types to balance progenitor cell retention and expansion with cell differentiation for evolution of tissue architecture. Underlying submandibular salivary gland branching morphogenesis is the regulated proliferation and differentiation of perhaps several progenitor cell populations, which have not been characterized throughout development, and yet are critical for understanding organ development, regeneration, and disease. Here we applied a serial multiplexed fluorescent immunohistochemistry technology to map the progressive refinement of the epithelial and mesenchymal cell populations throughout development from embryonic day 14 through postnatal day 20. Using computational single cell analysis methods, we simultaneously mapped the evolving temporal and spatial location of epithelial cells expressing subsets of differentiation and progenitor markers throughout salivary gland development. We mapped epithelial cell differentiation markers, including aquaporin 5, PSP, SABPA, and mucin 10 (acinar cells); cytokeratin 7 (ductal cells); and smooth muscle α-actin (myoepithelial cells) and epithelial progenitor cell markers, cytokeratin 5 and c-kit. We used pairwise correlation and visual mapping of the cells in multiplexed images to quantify the number of single- and double-positive cells expressing these differentiation and progenitor markers at each developmental stage. We identified smooth muscle α-actin as a putative early myoepithelial progenitor marker that is expressed in cytokeratin 5-negative cells. Additionally, our results reveal dynamic expansion and redistributions of c-kit- and K5-positive progenitor cell populations throughout development and in postnatal glands. The data suggest that there are temporally and spatially discreet progenitor populations that contribute to salivary gland development and homeostasis. |
| first_indexed | 2024-12-22T11:14:47Z |
| format | Article |
| id | doaj.art-f330b71b1b6944f7b3adfcb8fde714e6 |
| institution | Directory Open Access Journal |
| issn | 2046-6390 |
| language | English |
| last_indexed | 2024-12-22T11:14:47Z |
| publishDate | 2013-04-01 |
| publisher | The Company of Biologists |
| record_format | Article |
| series | Biology Open |
| spelling | doaj.art-f330b71b1b6944f7b3adfcb8fde714e62022-12-21T18:28:03ZengThe Company of BiologistsBiology Open2046-63902013-04-012543944710.1242/bio.2013430920134309Quantitative single cell analysis of cell population dynamics during submandibular salivary gland development and differentiationDeirdre A. Nelson0Charles Manhardt1Vidya Kamath2Yunxia Sui3Alberto Santamaria-Pang4Ali Can5Musodiq Bello6Alex Corwin7Sean R. Dinn8Michael Lazare9Elise M. Gervais10Sharon J. Sequeira11Sarah B. Peters12Fiona Ginty13Michael J. Gerdes14Melinda Larsen15 Department of Biological Sciences, University at Albany, State University of New York, 1400 Washington Avenue, Albany, NY 12222, USA Department of Biological Sciences, University at Albany, State University of New York, 1400 Washington Avenue, Albany, NY 12222, USA GE Global Research, One Research Circle, Niskayuna, NY 12309, USA GE Global Research, One Research Circle, Niskayuna, NY 12309, USA GE Global Research, One Research Circle, Niskayuna, NY 12309, USA GE Global Research, One Research Circle, Niskayuna, NY 12309, USA GE Global Research, One Research Circle, Niskayuna, NY 12309, USA GE Global Research, One Research Circle, Niskayuna, NY 12309, USA GE Global Research, One Research Circle, Niskayuna, NY 12309, USA Department of Biological Sciences, University at Albany, State University of New York, 1400 Washington Avenue, Albany, NY 12222, USA Department of Biological Sciences, University at Albany, State University of New York, 1400 Washington Avenue, Albany, NY 12222, USA Department of Biological Sciences, University at Albany, State University of New York, 1400 Washington Avenue, Albany, NY 12222, USA Department of Biological Sciences, University at Albany, State University of New York, 1400 Washington Avenue, Albany, NY 12222, USA GE Global Research, One Research Circle, Niskayuna, NY 12309, USA GE Global Research, One Research Circle, Niskayuna, NY 12309, USA Department of Biological Sciences, University at Albany, State University of New York, 1400 Washington Avenue, Albany, NY 12222, USA Summary Epithelial organ morphogenesis involves reciprocal interactions between epithelial and mesenchymal cell types to balance progenitor cell retention and expansion with cell differentiation for evolution of tissue architecture. Underlying submandibular salivary gland branching morphogenesis is the regulated proliferation and differentiation of perhaps several progenitor cell populations, which have not been characterized throughout development, and yet are critical for understanding organ development, regeneration, and disease. Here we applied a serial multiplexed fluorescent immunohistochemistry technology to map the progressive refinement of the epithelial and mesenchymal cell populations throughout development from embryonic day 14 through postnatal day 20. Using computational single cell analysis methods, we simultaneously mapped the evolving temporal and spatial location of epithelial cells expressing subsets of differentiation and progenitor markers throughout salivary gland development. We mapped epithelial cell differentiation markers, including aquaporin 5, PSP, SABPA, and mucin 10 (acinar cells); cytokeratin 7 (ductal cells); and smooth muscle α-actin (myoepithelial cells) and epithelial progenitor cell markers, cytokeratin 5 and c-kit. We used pairwise correlation and visual mapping of the cells in multiplexed images to quantify the number of single- and double-positive cells expressing these differentiation and progenitor markers at each developmental stage. We identified smooth muscle α-actin as a putative early myoepithelial progenitor marker that is expressed in cytokeratin 5-negative cells. Additionally, our results reveal dynamic expansion and redistributions of c-kit- and K5-positive progenitor cell populations throughout development and in postnatal glands. The data suggest that there are temporally and spatially discreet progenitor populations that contribute to salivary gland development and homeostasis.http://bio.biologists.org/content/2/5/439Salivary glandDevelopmentProgenitor cellsMultiplex analysis |
| spellingShingle | Deirdre A. Nelson Charles Manhardt Vidya Kamath Yunxia Sui Alberto Santamaria-Pang Ali Can Musodiq Bello Alex Corwin Sean R. Dinn Michael Lazare Elise M. Gervais Sharon J. Sequeira Sarah B. Peters Fiona Ginty Michael J. Gerdes Melinda Larsen Quantitative single cell analysis of cell population dynamics during submandibular salivary gland development and differentiation Biology Open Salivary gland Development Progenitor cells Multiplex analysis |
| title | Quantitative single cell analysis of cell population dynamics during submandibular salivary gland development and differentiation |
| title_full | Quantitative single cell analysis of cell population dynamics during submandibular salivary gland development and differentiation |
| title_fullStr | Quantitative single cell analysis of cell population dynamics during submandibular salivary gland development and differentiation |
| title_full_unstemmed | Quantitative single cell analysis of cell population dynamics during submandibular salivary gland development and differentiation |
| title_short | Quantitative single cell analysis of cell population dynamics during submandibular salivary gland development and differentiation |
| title_sort | quantitative single cell analysis of cell population dynamics during submandibular salivary gland development and differentiation |
| topic | Salivary gland Development Progenitor cells Multiplex analysis |
| url | http://bio.biologists.org/content/2/5/439 |
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