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Title: Perturbed myoepithelial cell differentiation in BRCA mutation carriers and in ductal carcinoma in situ

Abstract

Myoepithelial cells play key roles in normal mammary gland development and in limiting pre-invasive to invasive breast tumor progression, yet their differentiation and perturbation in ductal carcinoma in situ (DCIS) are poorly understood. Here, we investigated myoepithelial cells in normal breast tissues of BRCA1 and BRCA2 germline mutation carriers and in non-carrier controls, and in sporadic DCIS. We found that in the normal breast of non-carriers, myoepithelial cells frequently co-express the p63 and TCF7 transcription factors and that p63 and TCF7 show overlapping chromatin peaks associated with differentiated myoepithelium-specific genes. In contrast, in normal breast tissues of BRCA1 mutation carriers the frequency of p63+TCF7+ myoepithelial cells is significantly decreased and p63 and TCF7 chromatin peaks do not overlap. These myoepithelial perturbations in normal breast tissues of BRCA1 germline mutation carriers may play a role in their higher risk of breast cancer. The fraction of p63+TCF7+ myoepithelial cells is also significantly decreased in DCIS, which may be associated with invasive progression.

Authors:
 [1];  [2];  [3];  [4];  [5];  [5];  [6];  [7];  [8];  [9]; ORCiD logo [10];  [11]; ORCiD logo [8];  [5]; ORCiD logo [5];  [5];  [12];  [13];  [14];  [14] more »;  [14];  [14];  [15];  [12];  [12];  [16];  [17];  [18];  [19];  [20];  [19];  [19];  [19];  [19];  [21];  [22];  [14];  [23]; ORCiD logo [3]; ORCiD logo [24]; ORCiD logo [5];  [12];  [25];  [26]; ORCiD logo [27];  [28]; ORCiD logo [29];  [8] « less
+ Show Author Affiliations
  1. Harvard Medical School, Boston, MA (United States); Dana-Farber Cancer Inst., Boston, MA (United States)
  2. Deciphera Pharmaceuticals, Waltham, MA (United States); Harvard Medical School, Boston, MA (United States); Dana-Farber Cancer Inst., Boston, MA (United States)
  3. Harvard Medical School, Boston, MA (United States)
  4. Nagoya Univ. Graduate School of Medicine (Japan); Harvard Medical School, Boston, MA (United States); Dana-Farber Cancer Inst., Boston, MA (United States)
  5. Dana-Farber Cancer Inst., Boston, MA (United States)
  6. ImmunoGen, Inc., Waltham, MA (United States); Harvard Medical School, Boston, MA (United States)
  7. EMEA Site Intelligence and Activation, Tel Aviv (Israel); Dana-Farber Cancer Inst., Boston, MA (United States)
  8. Harvard Medical School, Boston, MA (United States); Dana-Farber Cancer Inst., Boston, MA (United States)
  9. WuXi NextCODE, Cambridge, MA (United States); Harvard Medical School, Boston, MA (United States); Dana-Farber Cancer Inst., Boston, MA (United States)
  10. Second Military Medical Univ., Shanghai (China); Yale Univ., New Haven, CT (United States)
  11. Univ. of New Mexico School of Medicine, Albuquerque, NM (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  12. Johns Hopkins Univ., Baltimore, MD (United States). School of Medicine
  13. Metamark Genetics, Inc., Worcester, MA (United States); Harvard Medical School, Boston, MA (United States); Dana-Farber Cancer Inst., Boston, MA (United States)
  14. Baylor-Charles A. Sammons Cancer Center, Dallas, TX (United States)
  15. Univ. of California San Francisco Helen Diller Family Comprehensive Cancer Center, CA (United States)
  16. Johns Hopkins Medical Institutions, Baltimore, MD (United States); Brigham and Women's Hospital (Harvard Medical School), Boston, MA (United States)
  17. Brigham and Women's Hospital (Harvard Medical School), Boston, MA (United States)
  18. Washington Univ. School of Medicine, St. Louis, MO (United States)
  19. Sutter Roseville Medical Center, Roseville, CA (United States)
  20. Cancer Treatment Centers of America, Atlanta, GA (United States); Sutter Roseville Medical Center, Roseville, CA (United States)
  21. Univ. of Michigan, Ann Arbor, MI (United States)
  22. Duke Univ., Durham, NC (United States); Univ. of California San Francisco Helen Diller Family Comprehensive Cancer Center, CA (United States)
  23. Harvard Univ., Cambridge, MA (United States); Harvard T. H. Chan School of Public Health, Boston, MA (United States); Dana-Farber Cancer Inst., Boston, MA (United States)
  24. Yale Univ., New Haven, CT (United States)
  25. Seoul National Univ. College of Medicine (Korea, Republic of)
  26. Brigham and Women's Hospital (Harvard Medical School), Boston, MA (United States); Dana-Farber Cancer Inst., Boston, MA (United States)
  27. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  28. MD Anderson Cancer Center, Houston, TX (United States)
  29. Harvard Stem Cell Inst., Cambridge, MA (United States); Dana-Farber Cancer Inst., Boston, MA (United States); Brigham and Women's Hospital (Harvard Medical School), Boston, MA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1572055
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Ding, Lina, Su, Ying, Fassl, Anne, Hinohara, Kunihiko, Qiu, Xintao, Harper, Nicholas W., Huh, Sung Jin, Bloushtain-Qimron, Noga, Jovanović, Bojana, Ekram, Muhammad, Zi, Xiaoyuan, Hines, William C., Alečković, Maša, Caulfield, Ryan J., Bonal, Dennis M., Nguyen, Quang-De, Merino, Vanessa F., Choudhury, Sibgat, Ethington, Gabrielle, Panos, Laura, Grant, Michael, Herlihy, William, Au, Alfred, Rosson, Gedge D., Argani, Pedram, Richardson, Andrea L., Dillon, Deborah, Allred, D. Craig, Babski, Kirsten, Kim, Elizabeth Min Hui, McDonnell, Charles H., Wagner, Jon, Rowberry, Ron, Bobolis, Kristie, Kleer, Celina G., Hwang, E. Shelley, Blum, Joanne L., Cristea, Simona, Sicinski, Piotr, Fan, Rong, Long, Henry W., Sukumar, Saraswati, Park, So Yeon, Garber, Judy E., Bissell, Mina, Yao, Jun, Polyak, Kornelia, and del Alcazar, Carlos Gil. Perturbed myoepithelial cell differentiation in BRCA mutation carriers and in ductal carcinoma in situ. United States: N. p., 2019. Web. doi:10.1038/s41467-019-12125-5.
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Ding, Lina, Su, Ying, Fassl, Anne, Hinohara, Kunihiko, Qiu, Xintao, Harper, Nicholas W., Huh, Sung Jin, Bloushtain-Qimron, Noga, Jovanović, Bojana, Ekram, Muhammad, Zi, Xiaoyuan, Hines, William C., Alečković, Maša, Caulfield, Ryan J., Bonal, Dennis M., Nguyen, Quang-De, Merino, Vanessa F., Choudhury, Sibgat, Ethington, Gabrielle, Panos, Laura, Grant, Michael, Herlihy, William, Au, Alfred, Rosson, Gedge D., Argani, Pedram, Richardson, Andrea L., Dillon, Deborah, Allred, D. Craig, Babski, Kirsten, Kim, Elizabeth Min Hui, McDonnell, Charles H., Wagner, Jon, Rowberry, Ron, Bobolis, Kristie, Kleer, Celina G., Hwang, E. Shelley, Blum, Joanne L., Cristea, Simona, Sicinski, Piotr, Fan, Rong, Long, Henry W., Sukumar, Saraswati, Park, So Yeon, Garber, Judy E., Bissell, Mina, Yao, Jun, Polyak, Kornelia, & del Alcazar, Carlos Gil. Perturbed myoepithelial cell differentiation in BRCA mutation carriers and in ductal carcinoma in situ. United States. https://doi.org/10.1038/s41467-019-12125-5
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Ding, Lina, Su, Ying, Fassl, Anne, Hinohara, Kunihiko, Qiu, Xintao, Harper, Nicholas W., Huh, Sung Jin, Bloushtain-Qimron, Noga, Jovanović, Bojana, Ekram, Muhammad, Zi, Xiaoyuan, Hines, William C., Alečković, Maša, Caulfield, Ryan J., Bonal, Dennis M., Nguyen, Quang-De, Merino, Vanessa F., Choudhury, Sibgat, Ethington, Gabrielle, Panos, Laura, Grant, Michael, Herlihy, William, Au, Alfred, Rosson, Gedge D., Argani, Pedram, Richardson, Andrea L., Dillon, Deborah, Allred, D. Craig, Babski, Kirsten, Kim, Elizabeth Min Hui, McDonnell, Charles H., Wagner, Jon, Rowberry, Ron, Bobolis, Kristie, Kleer, Celina G., Hwang, E. Shelley, Blum, Joanne L., Cristea, Simona, Sicinski, Piotr, Fan, Rong, Long, Henry W., Sukumar, Saraswati, Park, So Yeon, Garber, Judy E., Bissell, Mina, Yao, Jun, Polyak, Kornelia, and del Alcazar, Carlos Gil. Fri . "Perturbed myoepithelial cell differentiation in BRCA mutation carriers and in ductal carcinoma in situ". United States. https://doi.org/10.1038/s41467-019-12125-5. https://www.osti.gov/servlets/purl/1572055.
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@article{osti_1572055,
title = {Perturbed myoepithelial cell differentiation in BRCA mutation carriers and in ductal carcinoma in situ},
author = {Ding, Lina and Su, Ying and Fassl, Anne and Hinohara, Kunihiko and Qiu, Xintao and Harper, Nicholas W. and Huh, Sung Jin and Bloushtain-Qimron, Noga and Jovanović, Bojana and Ekram, Muhammad and Zi, Xiaoyuan and Hines, William C. and Alečković, Maša and Caulfield, Ryan J. and Bonal, Dennis M. and Nguyen, Quang-De and Merino, Vanessa F. and Choudhury, Sibgat and Ethington, Gabrielle and Panos, Laura and Grant, Michael and Herlihy, William and Au, Alfred and Rosson, Gedge D. and Argani, Pedram and Richardson, Andrea L. and Dillon, Deborah and Allred, D. Craig and Babski, Kirsten and Kim, Elizabeth Min Hui and McDonnell, Charles H. and Wagner, Jon and Rowberry, Ron and Bobolis, Kristie and Kleer, Celina G. and Hwang, E. Shelley and Blum, Joanne L. and Cristea, Simona and Sicinski, Piotr and Fan, Rong and Long, Henry W. and Sukumar, Saraswati and Park, So Yeon and Garber, Judy E. and Bissell, Mina and Yao, Jun and Polyak, Kornelia and del Alcazar, Carlos Gil},
abstractNote = {Myoepithelial cells play key roles in normal mammary gland development and in limiting pre-invasive to invasive breast tumor progression, yet their differentiation and perturbation in ductal carcinoma in situ (DCIS) are poorly understood. Here, we investigated myoepithelial cells in normal breast tissues of BRCA1 and BRCA2 germline mutation carriers and in non-carrier controls, and in sporadic DCIS. We found that in the normal breast of non-carriers, myoepithelial cells frequently co-express the p63 and TCF7 transcription factors and that p63 and TCF7 show overlapping chromatin peaks associated with differentiated myoepithelium-specific genes. In contrast, in normal breast tissues of BRCA1 mutation carriers the frequency of p63+TCF7+ myoepithelial cells is significantly decreased and p63 and TCF7 chromatin peaks do not overlap. These myoepithelial perturbations in normal breast tissues of BRCA1 germline mutation carriers may play a role in their higher risk of breast cancer. The fraction of p63+TCF7+ myoepithelial cells is also significantly decreased in DCIS, which may be associated with invasive progression.},
doi = {10.1038/s41467-019-12125-5},
journal = {Nature Communications},
number = 1,
volume = 10,
place = {United States},
year = {Fri Sep 13 00:00:00 EDT 2019},
month = {Fri Sep 13 00:00:00 EDT 2019}
}
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The importance of being a myoepithelial cell
journal, December 2002

  • Deugnier, Marie-Ange; Teulière, Jérôme; Faraldo, Marisa M.
  • Breast Cancer Research, Vol. 4, Issue 6
  • DOI: 10.1186/bcr459

The myoepithelial defense: a host defense against cancer
journal, January 1997

p63 in Epithelial Survival, Germ Cell Surveillance, and Neoplasia
journal, January 2010

ΔNp63 promotes stem cell activity in mammary gland development and basal-like breast cancer by enhancing Fzd7 expression and Wnt signalling
journal, September 2014

  • Chakrabarti, Rumela; Wei, Yong; Hwang, Julie
  • Nature Cell Biology, Vol. 16, Issue 10
  • DOI: 10.1038/ncb3040

Combined cDNA Array Comparative Genomic Hybridization and Serial Analysis of Gene Expression Analysis of Breast Tumor Progression
journal, April 2006

A Living Biobank of Breast Cancer Organoids Captures Disease Heterogeneity.
text, January 2018

Molecular characterization of the tumor microenvironment in breast cancer
journal, July 2004

Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers
journal, August 2009

  • Lim, Elgene; Vaillant, François; Wu, Di
  • Nature Medicine, Vol. 15, Issue 8
  • DOI: 10.1038/nm.2000

A method for quantifying normal human mammary epithelial stem cells with in vivo regenerative ability
journal, November 2008

  • Eirew, Peter; Stingl, John; Raouf, Afshin
  • Nature Medicine, Vol. 14, Issue 12
  • DOI: 10.1038/nm.1791

Organoids in immunological research
journal, December 2019

  • Bar-Ephraim, Yotam E.; Kretzschmar, Kai; Clevers, Hans
  • Nature Reviews Immunology, Vol. 20, Issue 5
  • DOI: 10.1038/s41577-019-0248-y

A Living Biobank of Breast Cancer Organoids Captures Disease Heterogeneity
journal, January 2018

p53/p63/p73 isoforms: an orchestra of isoforms to harmonise cell differentiation and response to stress
journal, April 2006

  • Murray-Zmijewski, F.; Lane, D. P.; Bourdon, J-C
  • Cell Death & Differentiation, Vol. 13, Issue 6
  • DOI: 10.1038/sj.cdd.4401914

BRCA1/FANCD2/BRG1-Driven DNA Repair Stabilizes the Differentiation State of Human Mammary Epithelial Cells
journal, July 2016

Cell type-specific DNA methylation patterns in the human breast
journal, September 2008

  • Bloushtain-Qimron, N.; Yao, J.; Snyder, E. L.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 37
  • DOI: 10.1073/pnas.0805206105

Role of COX-2 in epithelial-stromal cell interactions and progression of ductal carcinoma in situ of the breast
journal, February 2009

  • Hu, M.; Peluffo, G.; Chen, H.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 9
  • DOI: 10.1073/pnas.0813306106

Low CD10 mRNA Expression Identifies High-Risk Ductal Carcinoma In Situ (DCIS)
journal, August 2010

Target analysis by integration of transcriptome and ChIP-seq data with BETA
journal, November 2013

The mammary myoepithelial cell - Cinderella or ugly sister?
journal, February 2000

  • Lakhani, Sunil R.; O'Hare, Michael J.
  • Breast Cancer Research, Vol. 3, Issue 1
  • DOI: 10.1186/bcr260

Inactivation of Apc perturbs mammary development, but only directly results in acanthoma in the context of Tcf-1 deficiency
journal, September 2002

  • Gallagher, Ronald C. J.; Hay, Trevor; Meniel, Valerie
  • Oncogene, Vol. 21, Issue 42
  • DOI: 10.1038/sj.onc.1205892

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014

The CD10 Enzyme Is a Key Player to Identify and Regulate Human Mammary Stem Cells
journal, April 2010

  • Bachelard-Cascales, Elodie; Chapellier, Marion; Delay, Emmanuel
  • STEM CELLS, Vol. 28, Issue 6
  • DOI: 10.1002/stem.435

Normal and tumor-derived myoepithelial cells differ in their ability to interact with luminal breast epithelial cells for polarity and basement membrane deposition
journal, January 2002

  • Gudjonsson, Thorarinn; Rønnov-Jessen, Lone; Villadsen, René
  • Journal of Cell Science, Vol. 115, Issue 1
  • DOI: 10.1242/jcs.115.1.39
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    Loss of myoepithelial calponin‐1 characterizes high‐risk ductal carcinoma in situ cases, which are further stratified by T cell composition
    journal, March 2020

    • Mitchell, Elizabeth; Jindal, Sonali; Chan, Tiffany
    • Molecular Carcinogenesis, Vol. 59, Issue 7
    • DOI: 10.1002/mc.23171
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