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Title: Transcriptional changes associated with breast cancer occur as normal human mammary epithelial cells overcome senescence barriers and become immortalized

Abstract

Background: Human mammary epithelial cells (HMEC) overcome two well-characterized genetic and epigenetic barriers as they progress from primary cells to fully immortalized cell lines in vitro. Finite lifespan HMEC overcome an Rb-mediated stress-associated senescence barrier (stasis), and a stringent, telomere-length dependent, barrier (agonescence or crisis, depending on p53 status). HMEC that have overcome the second senescence barrier are immortalized. Methods: We have characterized pre-stasis, post-selection (post-stasis, with p16 silenced), and fully immortalized HMEC by transcription profiling and RT-PCR. Four pre-stasis and seven post-selection HMEC samples, along with 10 representatives of fully immortalized breast epithelial cell lines, were profiled using Affymetrix U133A/B chips and compared using both supervised and unsupervised clustering. Datasets were validated by RT-PCR for a select set of genes. Quantitative immunofluorescence was used to assess changes in transcriptional regulators associated with the gene expression changes. Results: The most dramatic and uniform changes we observed were in a set of about 30 genes that are characterized as a "cancer proliferation cluster," which includes genes expressed during mitosis (CDC2, CDC25, MCM2, PLK1) and following DNA damage. The increased expression of these genes was particularly concordant in the fully immortalized lines. Additional changes were observed in IFN-regulated genes in some post-selectionmore » and fully immortalized cultures. Nuclear localization was observed for several transcriptional regulators associated with expression of these genes in post-selection and immortalized HMEC, including Rb, Myc, BRCA1, HDAC3 and SP1. Conclusion: Gene expression profiles and cytological changes in related transcriptional regulators indicate that immortalized HMEC resemble non-invasive breast cancers, such as ductal and lobular carcinomas in situ, and are strikingly distinct from finite-lifespan HMEC, particularly with regard to genes involved in proliferation, cell cycle regulation, chromosome structure and the DNA damage response. The comparison of HMEC profiles with lines harboring oncogenic changes (e.g. overexpression of Her-2neu, loss of p53 expression) identifies genes involved in tissue remodeling as well as proinflamatory cytokines and S100 proteins. Studies on carcinogenesis using immortalized cell lines as starting points or "normal" controls need to account for the significant pre-existing genetic and epigenetic changes inherent in such lines before results can be broadly interpreted.« less

Authors:
 [1];  [2];  [1];  [2];  [3];  [3];  [1];  [3];  [3];  [4];  [2]
+ Show Author Affiliations
  1. Wyeth Research, Cambridge, MA (United States). Dept. of Biological Technologies. Section of Bioinformatics
  2. Wyeth Research, Cambridge, MA (United States). Dept. of Biological Technologies. Applied Genomics
  3. Wyeth Research, Cambridge, MA (United States). Dept. of Biological Technologies. Molecular Profiling and Biomarker Discovery
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division
Publication Date:
Research Org.:
Univ. of California, Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; US Dept. of Defense (DOD)
OSTI Identifier:
1626574
Grant/Contract Number:  
AC03-76SF00098; W81XWH-04-1-0580
Resource Type:
Accepted Manuscript
Journal Name:
Molecular Cancer
Additional Journal Information:
Journal Volume: 6; Journal Issue: 1; Journal ID: ISSN 1476-4598
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biochemistry & molecular biology; oncology; human mammary epithelial cell; immortalize cell line; psoriasin; high content screening; human mammary epithelial cell line

Citation Formats

Li, Yizheng, Pan, Jing, Li, Jian-Liang, Lee, Jee Hyung, Tunkey, Chris, Saraf, Katie, Garbe, James C., Whitley, Maryann Z., Jelinsky, Scott A., Stampfer, Martha R., and Haney, Steven A. Transcriptional changes associated with breast cancer occur as normal human mammary epithelial cells overcome senescence barriers and become immortalized. United States: N. p., 2007. Web. doi:10.1186/1476-4598-6-7.
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Li, Yizheng, Pan, Jing, Li, Jian-Liang, Lee, Jee Hyung, Tunkey, Chris, Saraf, Katie, Garbe, James C., Whitley, Maryann Z., Jelinsky, Scott A., Stampfer, Martha R., & Haney, Steven A. Transcriptional changes associated with breast cancer occur as normal human mammary epithelial cells overcome senescence barriers and become immortalized. United States. https://doi.org/10.1186/1476-4598-6-7
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Li, Yizheng, Pan, Jing, Li, Jian-Liang, Lee, Jee Hyung, Tunkey, Chris, Saraf, Katie, Garbe, James C., Whitley, Maryann Z., Jelinsky, Scott A., Stampfer, Martha R., and Haney, Steven A. Thu . "Transcriptional changes associated with breast cancer occur as normal human mammary epithelial cells overcome senescence barriers and become immortalized". United States. https://doi.org/10.1186/1476-4598-6-7. https://www.osti.gov/servlets/purl/1626574.
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@article{osti_1626574,
title = {Transcriptional changes associated with breast cancer occur as normal human mammary epithelial cells overcome senescence barriers and become immortalized},
author = {Li, Yizheng and Pan, Jing and Li, Jian-Liang and Lee, Jee Hyung and Tunkey, Chris and Saraf, Katie and Garbe, James C. and Whitley, Maryann Z. and Jelinsky, Scott A. and Stampfer, Martha R. and Haney, Steven A.},
abstractNote = {Background: Human mammary epithelial cells (HMEC) overcome two well-characterized genetic and epigenetic barriers as they progress from primary cells to fully immortalized cell lines in vitro. Finite lifespan HMEC overcome an Rb-mediated stress-associated senescence barrier (stasis), and a stringent, telomere-length dependent, barrier (agonescence or crisis, depending on p53 status). HMEC that have overcome the second senescence barrier are immortalized. Methods: We have characterized pre-stasis, post-selection (post-stasis, with p16 silenced), and fully immortalized HMEC by transcription profiling and RT-PCR. Four pre-stasis and seven post-selection HMEC samples, along with 10 representatives of fully immortalized breast epithelial cell lines, were profiled using Affymetrix U133A/B chips and compared using both supervised and unsupervised clustering. Datasets were validated by RT-PCR for a select set of genes. Quantitative immunofluorescence was used to assess changes in transcriptional regulators associated with the gene expression changes. Results: The most dramatic and uniform changes we observed were in a set of about 30 genes that are characterized as a "cancer proliferation cluster," which includes genes expressed during mitosis (CDC2, CDC25, MCM2, PLK1) and following DNA damage. The increased expression of these genes was particularly concordant in the fully immortalized lines. Additional changes were observed in IFN-regulated genes in some post-selection and fully immortalized cultures. Nuclear localization was observed for several transcriptional regulators associated with expression of these genes in post-selection and immortalized HMEC, including Rb, Myc, BRCA1, HDAC3 and SP1. Conclusion: Gene expression profiles and cytological changes in related transcriptional regulators indicate that immortalized HMEC resemble non-invasive breast cancers, such as ductal and lobular carcinomas in situ, and are strikingly distinct from finite-lifespan HMEC, particularly with regard to genes involved in proliferation, cell cycle regulation, chromosome structure and the DNA damage response. The comparison of HMEC profiles with lines harboring oncogenic changes (e.g. overexpression of Her-2neu, loss of p53 expression) identifies genes involved in tissue remodeling as well as proinflamatory cytokines and S100 proteins. Studies on carcinogenesis using immortalized cell lines as starting points or "normal" controls need to account for the significant pre-existing genetic and epigenetic changes inherent in such lines before results can be broadly interpreted.},
doi = {10.1186/1476-4598-6-7},
journal = {Molecular Cancer},
number = 1,
volume = 6,
place = {United States},
year = {Thu Jan 18 00:00:00 EST 2007},
month = {Thu Jan 18 00:00:00 EST 2007}
}
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    A lincRNA connected to cell mortality and epigenetically-silenced in most common human cancers
    journal, October 2015

    Single cell cytometry of protein function in RNAi treated cells and in native populations
    journal, August 2008

    The functional loss of the retinoblastoma tumour suppressor is a common event in basal-like and luminal B breast carcinomas
    journal, September 2008

    • Herschkowitz, Jason I.; He, Xiaping; Fan, Cheng
    • Breast Cancer Research, Vol. 10, Issue 5
    • DOI: 10.1186/bcr2142

    Analysis of the ways and methods of signaling pathways in regulating cell cycle of NIH3T3 at transcriptional level
    journal, October 2015

    Nucks1 synergizes with Trp53 to promote radiation lymphomagenesis in mice
    journal, August 2016

    Age and the means of bypassing stasis influence the intrinsic subtype of immortalized human mammary epithelial cells
    journal, March 2015

    • Lee, Jonathan K.; Garbe, James C.; Vrba, Lukas
    • Frontiers in Cell and Developmental Biology, Vol. 3
    • DOI: 10.3389/fcell.2015.00013

    BRCA1 in the DNA damage response and at telomeres
    journal, January 2013

    Processing of Human Reduction Mammoplasty and Mastectomy Tissues for Cell Culture
    journal, January 2013

    • LaBarge, Mark A.; Garbe, James C.; Stampfer, Martha R.
    • Journal of Visualized Experiments, Issue 71
    • DOI: 10.3791/50011
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