CCL5-Mediated Th2 Immune Polarization Promotes Metastasis in Luminal Breast Cancer

The tumor-promoting chemokine CCL5 has been implicated in malignant transformation of breast epithelial cells, with studies to date focusing mainly on basal-type breast cancers. In this study, we investigated the consequences of CCL5 deletion in the MMTV-PyMT transgenic mouse model of luminal breast...

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Vydáno v:Cancer research (Chicago, Ill.) Ročník 75; číslo 20; s. 4312 - 4321
Hlavní autoři: Zhang, Qianfei, Qin, Jilong, Zhong, Lin, Gong, Lei, Zhang, Bing, Zhang, Yan, Gao, Wei-Qiang
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States 15.10.2015
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ISSN:1538-7445
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Abstract The tumor-promoting chemokine CCL5 has been implicated in malignant transformation of breast epithelial cells, with studies to date focusing mainly on basal-type breast cancers. In this study, we investigated the consequences of CCL5 deletion in the MMTV-PyMT transgenic mouse model of luminal breast cancer. In this model, primary tumor burden and pulmonary metastases were reduced significantly in CCL5-deficient subjects, an effect found to be associated with a deficit of Th2 (IL4⁺CD4⁺ T) cells. Mechanistic investigations revealed that CCL5 activates CCR3, a highly expressed chemokine receptor on CD4⁺ T cells, and also boosts Gfi1 expression to promote the differentiation of Th2 cells, which enhance the prometastatic activity of tumor-associated myeloid cells. Clinically, polarization toward this immunosuppressive Th2 phenotype was also evident in patients with advanced luminal breast cancer. Thus, our findings showed that CCL5/CCR3 signaling promotes metastasis by inducing Th2 polarization of CD4⁺ T cells, with implications for prognosis and immunotherapy of luminal breast cancer.
AbstractList The tumor-promoting chemokine CCL5 has been implicated in malignant transformation of breast epithelial cells, with studies to date focusing mainly on basal-type breast cancers. In this study, we investigated the consequences of CCL5 deletion in the MMTV-PyMT transgenic mouse model of luminal breast cancer. In this model, primary tumor burden and pulmonary metastases were reduced significantly in CCL5-deficient subjects, an effect found to be associated with a deficit of Th2 (IL4⁺CD4⁺ T) cells. Mechanistic investigations revealed that CCL5 activates CCR3, a highly expressed chemokine receptor on CD4⁺ T cells, and also boosts Gfi1 expression to promote the differentiation of Th2 cells, which enhance the prometastatic activity of tumor-associated myeloid cells. Clinically, polarization toward this immunosuppressive Th2 phenotype was also evident in patients with advanced luminal breast cancer. Thus, our findings showed that CCL5/CCR3 signaling promotes metastasis by inducing Th2 polarization of CD4⁺ T cells, with implications for prognosis and immunotherapy of luminal breast cancer.
Author Gong, Lei
Gao, Wei-Qiang
Zhang, Bing
Zhang, Qianfei
Qin, Jilong
Zhang, Yan
Zhong, Lin
Author_xml – sequence: 1
  givenname: Qianfei
  surname: Zhang
  fullname: Zhang, Qianfei
  organization: State Key Laboratory of Oncogenes and Related Genes, Renji-Med X Clinical Stem Cell Research Center, Ren Ji Hospital, School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai, China
– sequence: 2
  givenname: Jilong
  surname: Qin
  fullname: Qin, Jilong
  organization: Department of Pathology, The First Affiliate Hospital of Guangzhou Medical University, Guangzhou, China
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  givenname: Lin
  surname: Zhong
  fullname: Zhong, Lin
  organization: Yuhuangding Hospital, Yantai, China
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  givenname: Lei
  surname: Gong
  fullname: Gong, Lei
  organization: Yuhuangding Hospital, Yantai, China
– sequence: 5
  givenname: Bing
  surname: Zhang
  fullname: Zhang, Bing
  organization: Department of Cardiology, Boston Children's Hospital, Boston, Massachusetts
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  givenname: Yan
  surname: Zhang
  fullname: Zhang, Yan
  email: gao.weiqiang@sjtu.edu.cn, yanzh@sjtu.edu.cn
  organization: State Key Laboratory of Oncogenes and Related Genes, Renji-Med X Clinical Stem Cell Research Center, Ren Ji Hospital, School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai, China. gao.weiqiang@sjtu.edu.cn yanzh@sjtu.edu.cn
– sequence: 7
  givenname: Wei-Qiang
  surname: Gao
  fullname: Gao, Wei-Qiang
  email: gao.weiqiang@sjtu.edu.cn, yanzh@sjtu.edu.cn
  organization: State Key Laboratory of Oncogenes and Related Genes, Renji-Med X Clinical Stem Cell Research Center, Ren Ji Hospital, School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai, China. Collarative Innovation Center of Systems Biomedicine, Sanghai, China. gao.weiqiang@sjtu.edu.cn yanzh@sjtu.edu.cn
BackLink https://www.ncbi.nlm.nih.gov/pubmed/26249173$$D View this record in MEDLINE/PubMed
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Snippet The tumor-promoting chemokine CCL5 has been implicated in malignant transformation of breast epithelial cells, with studies to date focusing mainly on...
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StartPage 4312
SubjectTerms Animals
Breast Neoplasms - genetics
Breast Neoplasms - immunology
Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Case-Control Studies
Cell Differentiation
Cell Transformation, Neoplastic - genetics
Cell Transformation, Neoplastic - metabolism
Chemokine CCL5 - blood
Chemokine CCL5 - deficiency
Chemokine CCL5 - genetics
Chemokine CCL5 - metabolism
Disease Models, Animal
Disease Progression
DNA-Binding Proteins - genetics
Female
Gene Deletion
Gene Expression
Humans
Interleukin-4 - genetics
Interleukin-4 - metabolism
Lung Neoplasms - secondary
Mice
Mice, Knockout
Myeloid Cells - immunology
Myeloid Cells - metabolism
Neoplasm Metastasis
Receptors, CCR3 - genetics
Receptors, CCR3 - metabolism
Signal Transduction
Spheroids, Cellular
T-Lymphocyte Subsets - cytology
T-Lymphocyte Subsets - immunology
T-Lymphocyte Subsets - metabolism
Th2 Cells - cytology
Th2 Cells - immunology
Th2 Cells - metabolism
Transcription Factors - genetics
Tumor Cells, Cultured
Title CCL5-Mediated Th2 Immune Polarization Promotes Metastasis in Luminal Breast Cancer
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