Breast cancer cells induce cancer-associated fibroblasts to secrete hepatocyte growth factor to enhance breast tumorigenesis
It has been well documented that microenvironment consisting of stroma affects breast cancer progression. However, the mechanisms by which cancer cells and fibroblasts, the major cell type in stroma, interact with each other during tumor development remains to be elucidated. Here, we show that the h...
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| description | It has been well documented that microenvironment consisting of stroma affects breast cancer progression. However, the mechanisms by which cancer cells and fibroblasts, the major cell type in stroma, interact with each other during tumor development remains to be elucidated. Here, we show that the human cancer-associated fibroblasts (CAFs) had higher activity in enhancing breast tumorigenecity compared to the normal tissue-associated fibroblasts (NAFs) isolated from the same patients. The expression level of hepatocyte growth factor (HGF) in these fibroblasts was positively correlated with their ability to enhance breast tumorigenesis in mice. Deprivation of HGF using a neutralizing antibody reduced CAF-mediated colony formation of human breast cancer cells, indicating that CAFs enhanced cancer cell colony formation mainly through HGF secretion. Co-culture with human breast cancer MDA-MB-468 cells in a transwell system enhanced NAFs to secret HGF as well as promote tumorigenecity. The newly gained ability of these "educated" NAFs became irreversible after continuing this process till fourth passage. These results suggested that breast cancer cells could alter the nature of its surrounding fibroblasts to secrete HGF to support its own progression through paracrine signaling. |
| doi_str_mv | 10.1371/journal.pone.0015313 |
| format | Article |
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However, the mechanisms by which cancer cells and fibroblasts, the major cell type in stroma, interact with each other during tumor development remains to be elucidated. Here, we show that the human cancer-associated fibroblasts (CAFs) had higher activity in enhancing breast tumorigenecity compared to the normal tissue-associated fibroblasts (NAFs) isolated from the same patients. The expression level of hepatocyte growth factor (HGF) in these fibroblasts was positively correlated with their ability to enhance breast tumorigenesis in mice. Deprivation of HGF using a neutralizing antibody reduced CAF-mediated colony formation of human breast cancer cells, indicating that CAFs enhanced cancer cell colony formation mainly through HGF secretion. Co-culture with human breast cancer MDA-MB-468 cells in a transwell system enhanced NAFs to secret HGF as well as promote tumorigenecity. 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These results suggested that breast cancer cells could alter the nature of its surrounding fibroblasts to secrete HGF to support its own progression through paracrine signaling.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0015313</identifier><identifier>PMID: 21249190</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Antibodies ; Biology ; Breast cancer ; Breast Neoplasms - pathology ; Cancer ; Cancer cells ; Cell culture ; Cell Line, Tumor ; Cell Transformation, Neoplastic - metabolism ; Chemokines ; Coculture Techniques ; Colonies ; Comparative analysis ; Deprivation ; Development and progression ; Disease Progression ; Female ; Fibroblasts ; Fibroblasts - pathology ; Fibroblasts - secretion ; Gene expression ; Genomics ; Growth factors ; Hepatocyte growth factor ; Hepatocyte Growth Factor - physiology ; Hepatocyte Growth Factor - secretion ; Humans ; Kinases ; Mammary Neoplasms, Animal - pathology ; Medical research ; Medicine ; Metastasis ; Mice ; Paracrine Communication ; Paracrine signalling ; Proteins ; Rodents ; Secretion ; Stroma ; Tumor Microenvironment - physiology ; Tumorigenesis</subject><ispartof>PloS one, 2011-01, Vol.6 (1), p.e15313</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Tyan et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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However, the mechanisms by which cancer cells and fibroblasts, the major cell type in stroma, interact with each other during tumor development remains to be elucidated. Here, we show that the human cancer-associated fibroblasts (CAFs) had higher activity in enhancing breast tumorigenecity compared to the normal tissue-associated fibroblasts (NAFs) isolated from the same patients. The expression level of hepatocyte growth factor (HGF) in these fibroblasts was positively correlated with their ability to enhance breast tumorigenesis in mice. Deprivation of HGF using a neutralizing antibody reduced CAF-mediated colony formation of human breast cancer cells, indicating that CAFs enhanced cancer cell colony formation mainly through HGF secretion. Co-culture with human breast cancer MDA-MB-468 cells in a transwell system enhanced NAFs to secret HGF as well as promote tumorigenecity. 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These results suggested that breast cancer cells could alter the nature of its surrounding fibroblasts to secrete HGF to support its own progression through paracrine signaling.</description><subject>Animals</subject><subject>Antibodies</subject><subject>Biology</subject><subject>Breast cancer</subject><subject>Breast Neoplasms - pathology</subject><subject>Cancer</subject><subject>Cancer cells</subject><subject>Cell culture</subject><subject>Cell Line, Tumor</subject><subject>Cell Transformation, Neoplastic - metabolism</subject><subject>Chemokines</subject><subject>Coculture Techniques</subject><subject>Colonies</subject><subject>Comparative analysis</subject><subject>Deprivation</subject><subject>Development and progression</subject><subject>Disease Progression</subject><subject>Female</subject><subject>Fibroblasts</subject><subject>Fibroblasts - pathology</subject><subject>Fibroblasts - secretion</subject><subject>Gene expression</subject><subject>Genomics</subject><subject>Growth factors</subject><subject>Hepatocyte growth factor</subject><subject>Hepatocyte Growth Factor - 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However, the mechanisms by which cancer cells and fibroblasts, the major cell type in stroma, interact with each other during tumor development remains to be elucidated. Here, we show that the human cancer-associated fibroblasts (CAFs) had higher activity in enhancing breast tumorigenecity compared to the normal tissue-associated fibroblasts (NAFs) isolated from the same patients. The expression level of hepatocyte growth factor (HGF) in these fibroblasts was positively correlated with their ability to enhance breast tumorigenesis in mice. Deprivation of HGF using a neutralizing antibody reduced CAF-mediated colony formation of human breast cancer cells, indicating that CAFs enhanced cancer cell colony formation mainly through HGF secretion. Co-culture with human breast cancer MDA-MB-468 cells in a transwell system enhanced NAFs to secret HGF as well as promote tumorigenecity. The newly gained ability of these "educated" NAFs became irreversible after continuing this process till fourth passage. These results suggested that breast cancer cells could alter the nature of its surrounding fibroblasts to secrete HGF to support its own progression through paracrine signaling.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21249190</pmid><doi>10.1371/journal.pone.0015313</doi><tpages>e15313</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Antibodies Biology Breast cancer Breast Neoplasms - pathology Cancer Cancer cells Cell culture Cell Line, Tumor Cell Transformation, Neoplastic - metabolism Chemokines Coculture Techniques Colonies Comparative analysis Deprivation Development and progression Disease Progression Female Fibroblasts Fibroblasts - pathology Fibroblasts - secretion Gene expression Genomics Growth factors Hepatocyte growth factor Hepatocyte Growth Factor - physiology Hepatocyte Growth Factor - secretion Humans Kinases Mammary Neoplasms, Animal - pathology Medical research Medicine Metastasis Mice Paracrine Communication Paracrine signalling Proteins Rodents Secretion Stroma Tumor Microenvironment - physiology Tumorigenesis |
| title | Breast cancer cells induce cancer-associated fibroblasts to secrete hepatocyte growth factor to enhance breast tumorigenesis |
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