Normal and tumor-derived myoepithelial cells differ in their ability to interact with luminal breast epithelial cells for polarity and basement membrane deposition
The signals that determine the correct polarity of breast epithelial structures in vivo are not understood. We have shown previously that luminal epithelial cells can be polarized when cultured within a reconstituted basement membrane gel. We reasoned that such cues in vivo may be given by myoepithe...
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Published in | Journal of cell science Vol. 115; no. Pt 1; pp. 39 - 50 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
England
01.01.2002
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Subjects | |
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Abstract | The signals that determine the correct polarity of breast epithelial structures in vivo are not understood. We have shown previously that luminal epithelial cells can be polarized when cultured within a reconstituted basement membrane gel. We reasoned that such cues in vivo may be given by myoepithelial cells. Accordingly, we used an assay where luminal epithelial cells are incorrectly polarized to test this hypothesis. We show that culturing human primary luminal epithelial cells within collagen-I gels leads to formation of structures with no lumina and with reverse polarity as judged by dual stainings for sialomucin, epithelial specific antigen or occludin. No basement membrane is deposited, and beta4-integrin staining is negative. Addition of purified human myoepithelial cells isolated from normal glands corrects the inverse polarity, and leads to formation of double-layered acini with central lumina. Among the laminins present in the human breast basement membrane (laminin-1, -5 and -10/11), laminin-1 was unique in its ability to substitute for myoepithelial cells in polarity reversal. Myoepithelial cells were purified also from four different breast cancer sources including a biphasic cell line. Three out of four samples either totally lacked the ability to interact with luminal epithelial cells, or conveyed only correction of polarity in a fraction of acini. This behavior was directly related to the ability of the tumor myoepithelial cells to produce alpha-1 chain of laminin. In vivo, breast carcinomas were either negative for laminin-1 (7/12 biopsies) or showed a focal, fragmented deposition of a less intensely stained basement membrane (5/12 biopsies). Dual staining with myoepithelial markers revealed that tumor-associated myoepithelial cells were either negative or weakly positive for expression of laminin-1, establishing a strong correlation between loss of laminin-1 and breast cancer. We conclude that the double-layered breast acinus may be recapitulated in culture and that one reason for the ability of myoepithelial cells to induce polarity is because they are the only source of laminin-1 in the breast in vivo. A further conclusion is that a majority of tumor-derived/-associated myoepithelial cells are deficient in their ability to impart polarity because they have lost their ability to synthesize sufficient or functional laminin-1. These results have important implications for the role of myoepithelial cells in maintenance of polarity in normal breast and how they may function as structural tumor suppressors. |
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AbstractList | The signals that determine the correct polarity of breast epithelial structures in vivo are not understood. We have shown previously that luminal epithelial cells can be polarized when cultured within a reconstituted basement membrane gel. We reasoned that such cues in vivo may be given by myoepithelial cells. Accordingly, we used an assay where luminal epithelial cells are incorrectly polarized to test this hypothesis. We show that culturing human primary luminal epithelial cells within collagen-I gels leads to formation of structures with no lumina and with reverse polarity as judged by dual stainings for sialomucin, epithelial specific antigen or occludin. No basement membrane is deposited, and β4-integrin staining is negative. Addition of purified human myoepithelial cells isolated from normal glands corrects the inverse polarity, and leads to formation of double-layered acini with central lumina. Among the laminins present in the human breast basement membrane (laminin-1, -5 and -10/11), laminin-1 was unique in its ability to substitute for myoepithelial cells in polarity reversal.
Myoepithelial cells were purified also from four different breast cancer sources including a biphasic cell line. Three out of four samples either totally lacked the ability to interact with luminal epithelial cells, or conveyed only correction of polarity in a fraction of acini. This behavior was directly related to the ability of the tumor myoepithelial cells to produce α-1 chain of laminin. In vivo, breast carcinomas were either negative for laminin-1 (7/12 biopsies) or showed a focal, fragmented deposition of a less intensely stained basement membrane (5/12 biopsies). Dual staining with myoepithelial markers revealed that tumor-associated myoepithelial cells were either negative or weakly positive for expression of laminin-1, establishing a strong correlation between loss of laminin-1 and breast cancer. We conclude that the double-layered breast acinus may be recapitulated in culture and that one reason for the ability of myoepithelial cells to induce polarity is because they are the only source of laminin-1 in the breast in vivo. A further conclusion is that a majority of tumor-derived/-associated myoepithelial cells are deficient in their ability to impart polarity because they have lost their ability to synthesize sufficient or functional laminin-1. These results have important implications for the role of myoepithelial cells in maintenance of polarity in normal breast and how they may function as structural tumor suppressors. The signals that determine the correct polarity of breast epithelial structures in vivo are not understood. We have shown previously that luminal epithelial cells can be polarized when cultured within a reconstituted basement membrane gel. We reasoned that such cues in vivo may be given by myoepithelial cells. Accordingly, we used an assay where luminal epithelial cells are incorrectly polarized to test this hypothesis. We show that culturing human primary luminal epithelial cells within collagen-I gels leads to formation of structures with no lumina and with reverse polarity as judged by dual stainings for sialomucin, epithelial specific antigen or occludin. No basement membrane is deposited, and beta4-integrin staining is negative. Addition of purified human myoepithelial cells isolated from normal glands corrects the inverse polarity, and leads to formation of double-layered acini with central lumina. Among the laminins present in the human breast basement membrane (laminin-1, -5 and -10/11), laminin-1 was unique in its ability to substitute for myoepithelial cells in polarity reversal. Myoepithelial cells were purified also from four different breast cancer sources including a biphasic cell line. Three out of four samples either totally lacked the ability to interact with luminal epithelial cells, or conveyed only correction of polarity in a fraction of acini. This behavior was directly related to the ability of the tumor myoepithelial cells to produce alpha-1 chain of laminin. In vivo, breast carcinomas were either negative for laminin-1 (7/12 biopsies) or showed a focal, fragmented deposition of a less intensely stained basement membrane (5/12 biopsies). Dual staining with myoepithelial markers revealed that tumor-associated myoepithelial cells were either negative or weakly positive for expression of laminin-1, establishing a strong correlation between loss of laminin-1 and breast cancer. We conclude that the double-layered breast acinus may be recapitulated in culture and that one reason for the ability of myoepithelial cells to induce polarity is because they are the only source of laminin-1 in the breast in vivo. A further conclusion is that a majority of tumor-derived/-associated myoepithelial cells are deficient in their ability to impart polarity because they have lost their ability to synthesize sufficient or functional laminin-1. These results have important implications for the role of myoepithelial cells in maintenance of polarity in normal breast and how they may function as structural tumor suppressors. |
Author | Petersen, Ole William Bissell, Mina J Gudjonsson, Thorarinn Rank, Fritz Rønnov-Jessen, Lone Villadsen, René |
AuthorAffiliation | 2 Zoophysiological Laboratory, The August Krogh Institute, DK-2100 Copenhagen Ø, Denmark 3 Department of Pathology, Rigshospitalet, DK-2100 Copenhagen Ø, Denmark 4 Life Sciences Division, Berkeley National Laboratory, Berkeley, CA 94720, USA 1 Structural Cell Biology Unit, Institute of Medical Anatomy, The Panum Institute, DK-2200 Copenhagen N, Denmark |
AuthorAffiliation_xml | – name: 4 Life Sciences Division, Berkeley National Laboratory, Berkeley, CA 94720, USA – name: 3 Department of Pathology, Rigshospitalet, DK-2100 Copenhagen Ø, Denmark – name: 2 Zoophysiological Laboratory, The August Krogh Institute, DK-2100 Copenhagen Ø, Denmark – name: 1 Structural Cell Biology Unit, Institute of Medical Anatomy, The Panum Institute, DK-2200 Copenhagen N, Denmark |
Author_xml | – sequence: 1 givenname: Thorarinn surname: Gudjonsson fullname: Gudjonsson, Thorarinn organization: Structural Cell Biology Unit, Institute of Medical Anatomy, The Panum Institute, DK-2200 Copenhagen N, Denmark – sequence: 2 givenname: Lone surname: Rønnov-Jessen fullname: Rønnov-Jessen, Lone – sequence: 3 givenname: René surname: Villadsen fullname: Villadsen, René – sequence: 4 givenname: Fritz surname: Rank fullname: Rank, Fritz – sequence: 5 givenname: Mina J surname: Bissell fullname: Bissell, Mina J – sequence: 6 givenname: Ole William surname: Petersen fullname: Petersen, Ole William |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/11801722$$D View this record in MEDLINE/PubMed |
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Snippet | The signals that determine the correct polarity of breast epithelial structures in vivo are not understood. We have shown previously that luminal epithelial... |
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StartPage | 39 |
SubjectTerms | Basement Membrane - metabolism Biomarkers - analysis Breast - cytology Breast - metabolism Breast - physiology Breast Neoplasms - metabolism Breast Neoplasms - pathology Carcinoma, Intraductal, Noninfiltrating - metabolism Carcinoma, Intraductal, Noninfiltrating - pathology Cell Differentiation Cell Polarity - physiology Collagen - physiology Epithelial Cells - metabolism Epithelial Cells - physiology Extracellular Matrix - chemistry Extracellular Matrix - physiology Female Fluorescent Antibody Technique Gels - chemistry Humans Immunohistochemistry Laminin - biosynthesis Laminin - immunology Microscopy, Confocal Tumor Cells, Cultured |
Title | Normal and tumor-derived myoepithelial cells differ in their ability to interact with luminal breast epithelial cells for polarity and basement membrane deposition |
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