Abrupt involution induces inflammation, estrogenic signaling, and hyperplasia linking lack of breastfeeding with increased risk of breast cancer.

Background: A large collaborative analysis of data from 47 epidemiological studies concluded that longer duration of breastfeeding reduces the risk of developing breast cancer. Despite the strong epidemiological evidence, the molecular mechanisms linking prolonged breastfeeding to decreased risk of...

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Published in:Breast Cancer Research Vol. 21; no. 1
Main Authors: Basree, Mustafa M., Shinde, Neelam, Koivisto, Christopher, Cuitino, Maria, Kladney, Raleigh, Zhang, Jianying, Stephens, Julie, Palettas, Marilly, Zhang, Allen, Kim, Hee Kyung, Acero-Bedoya, Santiago, Trimboli, Anthony, Stover, Daniel G., Ludwig, Thomas, Ganju, Ramesh, Weng, Daniel, Shields, Peter, Freudenheim, Jo, Leone, Gustavo W., Sizemore, Gina M.
Format: research Journal Article
Published: BioMed Central 7/17/2019
Online Access:View this record in EBSCOhost
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      dt: 7/17/2019
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      pub: BioMed Central
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        atl: Abrupt involution induces inflammation, estrogenic signaling, and hyperplasia linking lack of breastfeeding with increased risk of breast cancer.
      aug:
        au:
          Basree, Mustafa M.
          Shinde, Neelam
          Koivisto, Christopher
          Cuitino, Maria
          Kladney, Raleigh
          Zhang, Jianying
          Stephens, Julie
          Palettas, Marilly
          Zhang, Allen
          Kim, Hee Kyung
          Acero-Bedoya, Santiago
          Trimboli, Anthony
          Stover, Daniel G.
          Ludwig, Thomas
          Ganju, Ramesh
          Weng, Daniel
          Shields, Peter
          Freudenheim, Jo
          Leone, Gustavo W.
          Sizemore, Gina M.
        affil: The Comprehensive Cancer Center, College of Medicine, The Ohio State University, 460 West 12th Avenue, 43210, Columbus, OH, USA
      sug:
        subj:
          Breast Neoplasms Metabolism
          Inflammation Metabolism
          Signal Transduction
          Estrogens Metabolism
          Breast Feeding
          Breast Neoplasms Etiology
          Inflammation Complications
          Estrogens Adverse Effects
          Models, Biological
          Mice
          Immunohistochemistry
          Pregnancy
          Risk Factors
          Collagen Metabolism
          Proteins Metabolism
          Hyperplasia
          Human
          Animal Studies
          Steroids Metabolism
          Flow Cytometry
          Lactation
          Female
          Inflammation Pathology
          Breast Neoplasms Pathology
          Risk Assessment
          Epithelial Cells Metabolism
          Biopsy
          Disease Susceptibility
          Gene Expression Profiling
          Validation Studies
          Comparative Studies
          Evaluation Research
          Multicenter Studies
          Short Portable Mental Status Questionnaire
          Female
      ab: Background: A large collaborative analysis of data from 47 epidemiological studies concluded that longer duration of breastfeeding reduces the risk of developing breast cancer. Despite the strong epidemiological evidence, the molecular mechanisms linking prolonged breastfeeding to decreased risk of breast cancer remain poorly understood.Methods: We modeled two types of breastfeeding behaviors in wild type FVB/N mice: (1) normal or gradual involution of breast tissue following prolonged breastfeeding and (2) forced or abrupt involution following short-term breastfeeding. To accomplish this, pups were gradually weaned between 28 and 31 days (gradual involution) or abruptly at 7 days postpartum (abrupt involution). Mammary glands were examined for histological changes, proliferation, and inflammatory markers by immunohistochemistry. Fluorescence-activated cell sorting was used to quantify mammary epithelial subpopulations. Gene set enrichment analysis was used to analyze gene expression data from mouse mammary luminal progenitor cells. Similar analysis was done using gene expression data generated from human breast samples obtained from parous women enrolled on a tissue collection study, OSU-2011C0094, and were undergoing reduction mammoplasty without history of breast cancer.Results: Mammary glands from mice that underwent abrupt involution exhibited denser stroma, altered collagen composition, higher inflammation and proliferation, increased estrogen receptor α and progesterone receptor expression compared to those that underwent gradual involution. Importantly, when aged to 4 months postpartum, mice that were in the abrupt involution cohort developed ductal hyperplasia and squamous metaplasia. Abrupt involution also resulted in a significant expansion of the luminal progenitor cell compartment associated with enrichment of Notch and estrogen signaling pathway genes. Breast tissues obtained from healthy women who breastfed for < 6 months vs ≥ 6 months showed significant enrichment of Notch signaling pathway genes, along with a trend for enrichment for luminal progenitor gene signature similar to what is observed in BRCA1 mutation carriers and basal-like breast tumors.Conclusions: We report here for the first time that forced or abrupt involution of the mammary glands following pregnancy and lack of breastfeeding results in expansion of luminal progenitor cells, higher inflammation, proliferation, and ductal hyperplasia, a known risk factor for developing breast cancer.
      pubtype: Academic Journal
      doctype:
        research
        Journal Article
      ougenre: Article
    language: English
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