Age-related gene expression in luminal epithelial cells is driven by a microenvironment made from myoepithelial cells
Abstract
Luminal epithelial cells in the breast gradually alter gene and protein expression with age, appearing to lose lineage-specificity by acquiring myoepithelial-like characteristics. We hypothesize that the luminal lineage is particularly sensitive to microenvironment changes, and age-related microenvironment changes cause altered luminal cell phenotypes. To evaluate the effects of different microenvironments on the fidelity of epigenetically regulated luminal and myoepithelial gene expression, we generated a set of lineage-specific probes for genes that are controlled through DNA methylation. Culturing primary luminal cells under conditions that favor myoepithelial propogation led to their reprogramming at the level of gene methylation, and to a more myoepithelial-like expression profile. Primary luminal cells’ lineage-specific gene expression could be maintained when they were cultured as bilayers with primary myoepithelial cells. Isogenic stromal fibroblast co-cultures were unable to maintain the luminal phenotype. Mixed-age luminal-myoepithelial bilayers revealed that luminal cells adopt transcription and methylation patterns consistent with the chronological age of the myoepithelial cells. We provide evidence that the luminal epithelial phenotype is exquisitely sensitive to microenvironment conditions, and that states of aging are cell non-autonomously communicated through microenvironment cues over at least one cell diameter.
- Authors:
-
- City of Hope, Duarte, CA (United States). Dept. of Population Sciences
- City of Hope, Duarte, CA (United States). Dept. of Population Sciences; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division; Univ. of Birmingham (United Kingdom). Dept. of Environmental Bioinformatics
- City of Hope, Duarte, CA (United States). Dept. of Population Sciences; City of Hope, Duarte, CA (United States). Center for Cancer and Aging; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Univ. of Bergen (Norway). Center for Cancer Biomarkers Research
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1627972
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Aging
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 10; Journal ID: ISSN 1945-4589
- Publisher:
- Impact Journals
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Cell Biology; Geriatrics & Gerontology
Citation Formats
Miyano, Masaru, Sayaman, Rosalyn W., Stoiber, Marcus H., Lin, Chun-Han, Stampfer, Martha R., Brown, James B., and LaBarge, Mark A. Age-related gene expression in luminal epithelial cells is driven by a microenvironment made from myoepithelial cells. United States: N. p., 2017.
Web. doi:10.18632/aging.101298.
Miyano, Masaru, Sayaman, Rosalyn W., Stoiber, Marcus H., Lin, Chun-Han, Stampfer, Martha R., Brown, James B., & LaBarge, Mark A. Age-related gene expression in luminal epithelial cells is driven by a microenvironment made from myoepithelial cells. United States. https://doi.org/10.18632/aging.101298
Miyano, Masaru, Sayaman, Rosalyn W., Stoiber, Marcus H., Lin, Chun-Han, Stampfer, Martha R., Brown, James B., and LaBarge, Mark A. Mon .
"Age-related gene expression in luminal epithelial cells is driven by a microenvironment made from myoepithelial cells". United States. https://doi.org/10.18632/aging.101298. https://www.osti.gov/servlets/purl/1627972.
@article{osti_1627972,
title = {Age-related gene expression in luminal epithelial cells is driven by a microenvironment made from myoepithelial cells},
author = {Miyano, Masaru and Sayaman, Rosalyn W. and Stoiber, Marcus H. and Lin, Chun-Han and Stampfer, Martha R. and Brown, James B. and LaBarge, Mark A.},
abstractNote = {Luminal epithelial cells in the breast gradually alter gene and protein expression with age, appearing to lose lineage-specificity by acquiring myoepithelial-like characteristics. We hypothesize that the luminal lineage is particularly sensitive to microenvironment changes, and age-related microenvironment changes cause altered luminal cell phenotypes. To evaluate the effects of different microenvironments on the fidelity of epigenetically regulated luminal and myoepithelial gene expression, we generated a set of lineage-specific probes for genes that are controlled through DNA methylation. Culturing primary luminal cells under conditions that favor myoepithelial propogation led to their reprogramming at the level of gene methylation, and to a more myoepithelial-like expression profile. Primary luminal cells’ lineage-specific gene expression could be maintained when they were cultured as bilayers with primary myoepithelial cells. Isogenic stromal fibroblast co-cultures were unable to maintain the luminal phenotype. Mixed-age luminal-myoepithelial bilayers revealed that luminal cells adopt transcription and methylation patterns consistent with the chronological age of the myoepithelial cells. We provide evidence that the luminal epithelial phenotype is exquisitely sensitive to microenvironment conditions, and that states of aging are cell non-autonomously communicated through microenvironment cues over at least one cell diameter.},
doi = {10.18632/aging.101298},
journal = {Aging},
number = 10,
volume = 9,
place = {United States},
year = {Mon Oct 09 00:00:00 EDT 2017},
month = {Mon Oct 09 00:00:00 EDT 2017}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Muscle transplantation between young and old rats: age of host determines recovery
journal, June 1989
- Carlson, B. M.; Faulkner, J. A.
- American Journal of Physiology-Cell Physiology, Vol. 256, Issue 6
Gene expression profiles of human breast cancer progression
journal, April 2003
- Ma, X. -J.; Salunga, R.; Tuggle, J. T.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 10
Impact of aging on the biology of breast cancer
journal, April 2008
- Benz, Christopher C.
- Critical Reviews in Oncology/Hematology, Vol. 66, Issue 1
Methods that remove batch effects while retaining group differences may lead to exaggerated confidence in downstream analyses
journal, August 2015
- Nygaard, Vegard; Rødland, Einar Andreas; Hovig, Eivind
- Biostatistics, Vol. 17, Issue 1
Isolation, immortalization, and characterization of a human breast epithelial cell line with stem cell properties
journal, March 2002
- Gudjonsson, T.
- Genes & Development, Vol. 16, Issue 6
Life stage differences in mammary gland gene expression profile in non-human primates
text, January 2012
- Stute, Petra; Sielker, Sonja; Wood, Charles E.
- Springer US; http://www.springer-ny.com
Cell-cell and cell-matrix interactions differentially regulate the expression of hepatic and cytoskeletal genes in primary cultures of rat hepatocytes.
journal, April 1988
- Ben-Ze'ev, A.; Robinson, G. S.; Bucher, N. L.
- Proceedings of the National Academy of Sciences, Vol. 85, Issue 7
Aberrant Epigenetic Silencing Is Triggered by a Transient Reduction in Gene Expression
journal, March 2009
- Oyer, Jon A.; Chu, Adrian; Brar, Sukhmani
- PLoS ONE, Vol. 4, Issue 3
Use of within-array replicate spots for assessing differential expression in microarray experiments
journal, January 2005
- Smyth, G. K.; Michaud, J.; Scott, H. S.
- Bioinformatics, Vol. 21, Issue 9
Age-associated biomarker profiles of human breast cancer
journal, November 2002
- Eppenberger-Castori, Serenella; Moore, Dan H.; Thor, Ann D.
- The International Journal of Biochemistry & Cell Biology, Vol. 34, Issue 11
The sva package for removing batch effects and other unwanted variation in high-throughput experiments
journal, January 2012
- Leek, Jeffrey T.; Johnson, W. Evan; Parker, Hilary S.
- Bioinformatics, Vol. 28, Issue 6
lumi: a pipeline for processing Illumina microarray
journal, May 2008
- Du, P.; Kibbe, W. A.; Lin, S. M.
- Bioinformatics, Vol. 24, Issue 13
The NIH Roadmap Epigenomics Mapping Consortium
journal, October 2010
- Bernstein, Bradley E.; Stamatoyannopoulos, John A.; Costello, Joseph F.
- Nature Biotechnology, Vol. 28, Issue 10
Human Mammary Luminal Epithelial Cells Contain Progenitors to Myoepithelial Cells
journal, February 1999
- Péchoux, Christine; Gudjonsson, Thorarinn; Rønnov-Jessen, Lone
- Developmental Biology, Vol. 206, Issue 1
Epigenetically reprogramming metastatic tumor cells with an embryonic microenvironment
journal, December 2009
- Costa, Fabricio F.; Seftor, Elisabeth A.; Bischof, Jared M.
- Epigenomics, Vol. 1, Issue 2
The Polycomb complex PRC2 and its mark in life
journal, January 2011
- Margueron, Raphaël; Reinberg, Danny
- Nature, Vol. 469, Issue 7330
Age-Specific Changes in Intrinsic Breast Cancer Subtypes: A Focus on Older Women
journal, August 2014
- Jenkins, E. O.; Deal, A. M.; Anders, C. K.
- The Oncologist, Vol. 19, Issue 10
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
Adjusting batch effects in microarray expression data using empirical Bayes methods
journal, April 2006
- Johnson, W. Evan; Li, Cheng; Rabinovic, Ariel
- Biostatistics, Vol. 8, Issue 1
Elf5 Regulates Mammary Gland Stem/Progenitor Cell Fate by Influencing Notch Signaling
journal, June 2012
- Chakrabarti, Rumela; Wei, Yong; Romano, Rose-Anne
- STEM CELLS, Vol. 30, Issue 7
Aging and Gene Expression in the Primate Brain
journal, August 2005
- Fraser, Hunter B.; Khaitovich, Philipp; Plotkin, Joshua B.
- PLoS Biology, Vol. 3, Issue 9
Meta-analysis of age-related gene expression profiles identifies common signatures of aging
journal, February 2009
- de Magalhães, João Pedro; Curado, João; Church, George M.
- Bioinformatics, Vol. 25, Issue 7
Breast Cancer beyond the Age of Mutation
journal, November 2015
- LaBarge, Mark A.; Mora-Blanco, E. Lorena; Samson, Susan
- Gerontology, Vol. 62, Issue 4
Optimizing the noise versus bias trade-off for Illumina whole genome expression BeadChips
journal, October 2010
- Shi, Wei; Oshlack, Alicia; Smyth, Gordon K.
- Nucleic Acids Research, Vol. 38, Issue 22
Notch-Mediated Restoration of Regenerative Potential to Aged Muscle
journal, November 2003
- Conboy, Irina M.; Conboy, Michael J.; Smythe, Gayle M.
- Science, Vol. 302, Issue 5650
Multivalent epigenetic marks confer microenvironment-responsive epigenetic plasticity to ovarian cancer cells
journal, November 2010
- Bapat, Sharmila A.; Jin, Victor; Berry, Nicholas
- Epigenetics, Vol. 5, Issue 8
Sustained activation of STAT5 is essential for chromatin remodeling and maintenance of mammary-specific function
journal, January 2009
- Xu, Ren; Nelson, Celeste M.; Muschler, John L.
- The Journal of Cell Biology, Vol. 184, Issue 1
Transcriptional profiling of aging in human muscle reveals a common aging signature
journal, January 2005
- Zahn, Jacob M.; Sonu, Rebecca; Vogel, Hannes
- PLoS Genetics, Vol. preprint, Issue 2006
Pvclust: an R package for assessing the uncertainty in hierarchical clustering
journal, April 2006
- Suzuki, R.; Shimodaira, H.
- Bioinformatics, Vol. 22, Issue 12
Myoepithelial cells: good fences make good neighbors
journal, July 2005
- Adriance, Melissa C.; Inman, Jamie L.; Petersen, Ole W.
- Breast Cancer Research, Vol. 7, Issue 5
limma powers differential expression analyses for RNA-sequencing and microarray studies
journal, January 2015
- Ritchie, Matthew E.; Phipson, Belinda; Wu, Di
- Nucleic Acids Research, Vol. 43, Issue 7
Histone methylation: a dynamic mark in health, disease and inheritance
journal, April 2012
- Greer, Eric L.; Shi, Yang
- Nature Reviews Genetics, Vol. 13, Issue 5
Distinct DNA methylation changes highly correlated with chronological age in the human brain
journal, January 2011
- Hernandez, Dena G.; Nalls, Michael A.; Gibbs, J. Raphael
- Human Molecular Genetics, Vol. 20, Issue 6
Aging impacts transcriptomes but not genomes of hormone-dependent breast cancers
journal, September 2007
- Yau, Christina; Fedele, Vita; Roydasgupta, Ritu
- Breast Cancer Research, Vol. 9, Issue 5
Myoepithelial Cells: Their Origin and Function in Breast Morphogenesis and Neoplasia
journal, July 2005
- Gudjonsson, Thorarinn; Adriance, Melissa C.; Sternlicht, Mark D.
- Journal of Mammary Gland Biology and Neoplasia, Vol. 10, Issue 3
Impact of aging on the biology of breast cancer
journal, April 2008
- Benz, Christopher C.
- Critical Reviews in Oncology/Hematology, Vol. 66, Issue 1
Age-Dependent Changes in Breast Cancer Hormone Receptors and Oxidant Stress Markers
journal, December 2002
- Quong, Judy; Eppenberger-Castori, Serenella; Moore, Dan
- Breast Cancer Research and Treatment, Vol. 76, Issue 3
Age-Related Dysfunction in Mechanotransduction Impairs Differentiation of Human Mammary Epithelial Progenitors
journal, June 2014
- Pelissier, Fanny A.; Garbe, James C.; Ananthanarayanan, Badriprasad
- Cell Reports, Vol. 7, Issue 6
Meta-analysis of age-related gene expression profiles identifies common signatures of aging
journal, February 2009
- de Magalhães, João Pedro; Curado, João; Church, George M.
- Bioinformatics, Vol. 25, Issue 7
Transcriptional Profiling of Aging in Human Muscle Reveals a Common Aging Signature
journal, July 2006
- Zahn, Jacob M.; Sonu, Rebecca; Vogel, Hannes
- PLoS Genetics, Vol. 2, Issue 7
Aging and Gene Expression in the Primate Brain
journal, August 2005
- Fraser, Hunter B.; Khaitovich, Philipp; Plotkin, Joshua B.
- PLoS Biology, Vol. 3, Issue 9
Genome‐wideDNA methylation changes with age in disease‐free human skeletal muscle
journal, December 2013
- Zykovich, Artem; Hubbard, Alan; Flynn, James M.
- Aging Cell, Vol. 13, Issue 2
Genome-wide Methylation Profiles Reveal Quantitative Views of Human Aging Rates
journal, January 2013
- Hannum, Gregory; Guinney, Justin; Zhao, Ling
- Molecular Cell, Vol. 49, Issue 2
Distinct DNA methylation changes highly correlated with chronological age in the human brain
journal, January 2011
- Hernandez, Dena G.; Nalls, Michael A.; Gibbs, J. Raphael
- Human Molecular Genetics, Vol. 20, Issue 6
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
Modulation of secreted proteins of mouse mammary epithelial cells by the collagenous substrata
journal, January 1984
- Lee, E. Y.
- The Journal of Cell Biology, Vol. 98, Issue 1
Cell-cell and cell-matrix interactions differentially regulate the expression of hepatic and cytoskeletal genes in primary cultures of rat hepatocytes.
journal, April 1988
- Ben-Ze'ev, A.; Robinson, G. S.; Bucher, N. L.
- Proceedings of the National Academy of Sciences, Vol. 85, Issue 7
Notch-Mediated Restoration of Regenerative Potential to Aged Muscle
journal, November 2003
- Conboy, Irina M.; Conboy, Michael J.; Smythe, Gayle M.
- Science, Vol. 302, Issue 5650
The NIH Roadmap Epigenomics Mapping Consortium
journal, October 2010
- Bernstein, Bradley E.; Stamatoyannopoulos, John A.; Costello, Joseph F.
- Nature Biotechnology, Vol. 28, Issue 10
Sustained activation of STAT5 is essential for chromatin remodeling and maintenance of mammary-specific function
journal, January 2009
- Xu, Ren; Nelson, Celeste M.; Muschler, John L.
- The Journal of Cell Biology, Vol. 184, Issue 1
ELF5 Suppresses Estrogen Sensitivity and Underpins the Acquisition of Antiestrogen Resistance in Luminal Breast Cancer
journal, December 2012
- Kalyuga, Maria; Gallego-Ortega, David; Lee, Heather J.
- PLoS Biology, Vol. 10, Issue 12
Myoepithelial cells: good fences make good neighbors
journal, July 2005
- Adriance, Melissa C.; Inman, Jamie L.; Petersen, Ole W.
- Breast Cancer Research, Vol. 7, Issue 5
Breast Cancer beyond the Age of Mutation
journal, November 2015
- LaBarge, Mark A.; Mora-Blanco, E. Lorena; Samson, Susan
- Gerontology, Vol. 62, Issue 4
Epigenetically reprogramming metastatic tumor cells with an embryonic microenvironment
journal, December 2009
- Costa, Fabricio F.; Seftor, Elisabeth A.; Bischof, Jared M.
- Epigenomics, Vol. 1, Issue 2
Relationship between expression and methylation status of p16INK4a and the proliferative activity of different areas’ tumour cells in human colorectal cancer
journal, May 2007
- Jie, G.; Zhixiang, S.; Lei, S.
- International Journal of Clinical Practice, Vol. 61, Issue 9
The 3D tissue microenvironment modulates DNA methylation and E-cadherin expression in squamous cell carcinoma
journal, January 2012
- DesRochers, Teresa M.; Shamis, Yulia; Alt-Holland, Addy
- Epigenetics, Vol. 7, Issue 1
Multivalent epigenetic marks confer microenvironment-responsive epigenetic plasticity to ovarian cancer cells
journal, November 2010
- Bapat, Sharmila A.; Jin, Victor; Berry, Nicholas
- Epigenetics, Vol. 5, Issue 8
Aberrant Epigenetic Silencing Is Triggered by a Transient Reduction in Gene Expression
journal, March 2009
- Oyer, Jon A.; Chu, Adrian; Brar, Sukhmani
- PLoS ONE, Vol. 4, Issue 3
Histone methylation: a dynamic mark in health, disease and inheritance
journal, April 2012
- Greer, Eric L.; Shi, Yang
- Nature Reviews Genetics, Vol. 13, Issue 5
The Polycomb complex PRC2 and its mark in life
journal, January 2011
- Margueron, Raphaël; Reinberg, Danny
- Nature, Vol. 469, Issue 7330
DNA methylation patterns and epigenetic memory
journal, January 2002
- Bird, A.
- Genes & Development, Vol. 16, Issue 1
Rejuvenation of aged progenitor cells by exposure to a young systemic environment
journal, February 2005
- Conboy, Irina M.; Conboy, Michael J.; Wagers, Amy J.
- Nature, Vol. 433, Issue 7027
Growth Differentiation Factor 11 Is a Circulating Factor that Reverses Age-Related Cardiac Hypertrophy
journal, May 2013
- Loffredo, Francesco S.; Steinhauser, Matthew L.; Jay, Steven M.
- Cell, Vol. 153, Issue 4
Rejuvenation of Regeneration in the Aging Central Nervous System
journal, January 2012
- Ruckh, Julia M.; Zhao, Jing-Wei; Shadrach, Jennifer L.
- Cell Stem Cell, Vol. 10, Issue 1
Life stage differences in mammary gland gene expression profile in non-human primates
journal, October 2011
- Stute, Petra; Sielker, Sonja; Wood, Charles E.
- Breast Cancer Research and Treatment, Vol. 133, Issue 2
Elf5 is essential for early embryogenesis and mammary gland development during pregnancy and lactation
journal, January 2005
- Zhou, Jiong; Chehab, Renee; Tkalcevic, Josephine
- The EMBO Journal, Vol. 24, Issue 3
Elf5 Regulates Mammary Gland Stem/Progenitor Cell Fate by Influencing Notch Signaling
journal, June 2012
- Chakrabarti, Rumela; Wei, Yong; Romano, Rose-Anne
- STEM CELLS, Vol. 30, Issue 7
Elf5 inhibits the epithelial–mesenchymal transition in mammary gland development and breast cancer metastasis by transcriptionally repressing Snail2
journal, October 2012
- Chakrabarti, Rumela; Hwang, Julie; Andres Blanco, Mario
- Nature Cell Biology, Vol. 14, Issue 11
Gene expression profiles of human breast cancer progression
journal, April 2003
- Ma, X. -J.; Salunga, R.; Tuggle, J. T.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 10
Aging impacts transcriptomes but not genomes of hormone-dependent breast cancers
journal, September 2007
- Yau, Christina; Fedele, Vita; Roydasgupta, Ritu
- Breast Cancer Research, Vol. 9, Issue 5
Age-Specific Changes in Intrinsic Breast Cancer Subtypes: A Focus on Older Women
journal, August 2014
- Jenkins, E. O.; Deal, A. M.; Anders, C. K.
- The Oncologist, Vol. 19, Issue 10
Isolation, immortalization, and characterization of a human breast epithelial cell line with stem cell properties
journal, March 2002
- Gudjonsson, T.
- Genes & Development, Vol. 16, Issue 6
Human Mammary Luminal Epithelial Cells Contain Progenitors to Myoepithelial Cells
journal, February 1999
- Péchoux, Christine; Gudjonsson, Thorarinn; Rønnov-Jessen, Lone
- Developmental Biology, Vol. 206, Issue 1
Molecular Distinctions between Stasis and Telomere Attrition Senescence Barriers Shown by Long-term Culture of Normal Human Mammary Epithelial Cells
journal, September 2009
- Garbe, J. C.; Bhattacharya, S.; Merchant, B.
- Cancer Research, Vol. 69, Issue 19
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
Optimizing the noise versus bias trade-off for Illumina whole genome expression BeadChips
journal, October 2010
- Shi, Wei; Oshlack, Alicia; Smyth, Gordon K.
- Nucleic Acids Research, Vol. 38, Issue 22
limma powers differential expression analyses for RNA-sequencing and microarray studies
journal, January 2015
- Ritchie, Matthew E.; Phipson, Belinda; Wu, Di
- Nucleic Acids Research, Vol. 43, Issue 7
Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis
journal, November 2010
- Du, Pan; Zhang, Xiao; Huang, Chiang-Ching
- BMC Bioinformatics, Vol. 11, Issue 1
lumi: a pipeline for processing Illumina microarray
journal, May 2008
- Du, P.; Kibbe, W. A.; Lin, S. M.
- Bioinformatics, Vol. 24, Issue 13
Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments
journal, January 2004
- Smyth, Gordon K.
- Statistical Applications in Genetics and Molecular Biology, Vol. 3, Issue 1
Use of within-array replicate spots for assessing differential expression in microarray experiments
journal, January 2005
- Smyth, G. K.; Michaud, J.; Scott, H. S.
- Bioinformatics, Vol. 21, Issue 9
Adjusting batch effects in microarray expression data using empirical Bayes methods
journal, April 2006
- Johnson, W. Evan; Li, Cheng; Rabinovic, Ariel
- Biostatistics, Vol. 8, Issue 1
The sva package for removing batch effects and other unwanted variation in high-throughput experiments
journal, January 2012
- Leek, Jeffrey T.; Johnson, W. Evan; Parker, Hilary S.
- Bioinformatics, Vol. 28, Issue 6
Methods that remove batch effects while retaining group differences may lead to exaggerated confidence in downstream analyses
journal, August 2015
- Nygaard, Vegard; Rødland, Einar Andreas; Hovig, Eivind
- Biostatistics, Vol. 17, Issue 1
Pvclust: an R package for assessing the uncertainty in hierarchical clustering
journal, April 2006
- Suzuki, R.; Shimodaira, H.
- Bioinformatics, Vol. 22, Issue 12
Works referencing / citing this record:
Application of the D492 Cell Lines to Explore Breast Morphogenesis, EMT and Cancer Progression in 3D Culture
journal, January 2019
- Briem, Eirikur; Ingthorsson, Saevar; Traustadottir, Gunnhildur Asta
- Journal of Mammary Gland Biology and Neoplasia, Vol. 24, Issue 2
Transcriptional regulation of normal human mammary cell heterogeneity and its perturbation in breast cancer
journal, January 2019
- Pellacani, Davide; Tan, Susanna; Lefort, Sylvain
- The EMBO Journal, Vol. 38, Issue 14
Expression of Myoepithelial Markers in Mammary Carcinomas of 119 Pet Rabbits
journal, September 2019
- Degner, Sophie; Schoon, Heinz-Adolf; Degner, Sebastian
- Animals, Vol. 9, Issue 10
Application of the D492 Cell Lines to Explore Breast Morphogenesis, EMT and Cancer Progression in 3D Culture
journal, January 2019
- Briem, Eirikur; Ingthorsson, Saevar; Traustadottir, Gunnhildur Asta
- Journal of Mammary Gland Biology and Neoplasia, Vol. 24, Issue 2
Different culture media modulate growth, heterogeneity, and senescence in human mammary epithelial cell cultures
journal, October 2018
- Lee, Jonathan K.; Bloom, Jessica; Zubeldia-Plazaola, Arantzazu
- PLOS ONE, Vol. 13, Issue 10
Breast Tissue Biology Expands the Possibilities for Prevention of Age-Related Breast Cancers
journal, August 2019
- Fresques, Tara; Zirbes, Arrianna; Shalabi, Sundus
- Frontiers in Cell and Developmental Biology, Vol. 7