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PMID: 23959857 Published · ppublish English Journal Article

Obesity promotes breast cancer by CCL2-mediated macrophage recruitment and angiogenesis.

Cancer research ·Vol. 73 ·No. 19 ·2013-10-01 ·Pages 6080-93

Arendt LM, McCready J, Keller PJ, Baker DD, Naber SP, Seewaldt V, Kuperwasser C

Abstract

Obesity is one of the most important preventable causes of cancer and the most significant risk factor for breast cancer in postmenopausal women. Compared with lean women, obese women are more likely to be diagnosed with a larger, higher grade tumor, an increased incidence of lymph node metastases, and elevated risk of distant recurrence. However, the mechanisms connecting obesity to the pathogenesis of breast cancer are poorly defined. Here, we show that during obesity, adipocytes within human and mouse breast tissues recruit and activate macrophages through a previously uncharacterized CCL2/IL-1β/CXCL12 signaling pathway. Activated macrophages in turn promote stromal vascularization and angiogenesis even before the formation of cancer. Recapitulating these changes using a novel humanized breast cancer model was sufficient to promote angiogenesis and prime the microenvironment prior to neoplastic transformation for accelerated breast oncogenesis. These findings provide a mechanistic role for adipocytes and macrophages before carcinogenesis that may be critical for prevention and treatment of obesity-related cancer.

MeSH Terms
Adipocytes/metabolism,pathology Animals Apoptosis Blotting, Western Breast/metabolism,pathology Breast Neoplasms/etiology,metabolism,pathology Cattle Cell Differentiation Cell Movement Cell Proliferation Cells, Cultured Chemokine CCL2/genetics,metabolism Chemokine CXCL12/metabolism Endothelium, Vascular/cytology,metabolism Female Fluorescent Antibody Technique Humans Immunoenzyme Techniques Immunoprecipitation Interleukin-1beta/metabolism Macrophages/metabolism,pathology Mammary Glands, Animal/metabolism,pathology Mice Mice, Inbred C57BL Mice, Inbred NOD Mice, SCID Neovascularization, Pathologic Obesity/complications,metabolism,pathology Retina/cytology,metabolism Tumor Microenvironment
Chemicals
Ccl2 protein, mouse Chemokine CCL2 Chemokine CXCL12 Cxcl12 protein, mouse Interleukin-1beta
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Arendt Lisa M
Authors' Affiliations: Developmental, Molecular, and Chemical Biology Department, Sackler School of Graduate Biomedical Sciences, Tufts University School of Medicine; Molecular Oncology Research Institute and Medical Oncology and Department of Pathology, Tufts Medical Center, Boston, Massachusetts; and Departments of Medicine, Duke University, Durham, North Carolina.
McCready Jessica
Keller Patricia J
Baker Dana D
Naber Stephen P
Seewaldt Victoria
Kuperwasser Charlotte
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Article Info
Journal
Cancer research
Abbr.
Cancer Res
ISSN
1538-7445
Published
2013-10-01
Epub
2013-00-19
Pages
6080-93
Language
English
Region
United States
NLM ID
2984705R
PMCID
PMC3824388
Subset
IM
Grants
NCI NIH HHS · P01 CA092644 · United States
NCRR NIH HHS · K01 RR021858 · United States
NCI NIH HHS · R01 CA170851 · United States
NICHD NIH HHS · R01 HD073035 · United States
NIGMS NIH HHS · K12 GM074869 · United States
NCI NIH HHS · R01 CA125554 · United States
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