Modelling breast cancer requires identification and correction of a critical cell lineage-dependent transduction bias

Hines, William C.; Yaswen, Paul; Bissell, Mina J.

doi:10.1038/ncomms7927

Title: Modelling breast cancer requires identification and correction of a critical cell lineage-dependent transduction bias

Journal Article · Tue Apr 21 00:00:00 EDT 2015 · Nature Communications

DOI:https://doi.org/10.1038/ncomms7927· OSTI ID:1256019

Hines, William C. ^[1]; Yaswen, Paul ^[1]; Bissell, Mina J. ^[1]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

When trying to explore the biology and etiology of human cancers, clinically relevant human culture models are essential. Current breast tumour models, such as those from oncogenically transformed primary breast cells, produce predominantly basal-like properties, whereas the more common phenotype expressed by the vast majority of breast tumours are luminal. Reasons for this puzzling, yet important phenomenon, are not understood. We show here that luminal epithelial cells are significantly more resistant to viral transduction than their myoepithelial counterparts. Here, we suggest that this is a significant barrier to generating luminal cell lines and experimental tumours in vivo and to accurate interpretation of results. We show that the resistance is due to lower affinity of luminal cells for virus attachment, which can be overcome by pretreating cells—or virus—with neuraminidase. We present an analytical method for quantifying transductional differences between cell types and an optimized protocol for transducing unsorted primary human breast cells in context.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH1123; U01CA143233; U54CA112970; R01CA140663; R37CA064786

OSTI ID:: 1256019

Journal Information:: Nature Communications, Vol. 6; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 14 works

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References (39)

Choosing a Mouse Model: Experimental Biology in Context--The Utility and Limitations of Mouse Models of Breast Cancer Borowsky, A. D. Cold Spring Harbor Perspectives in Biology, Vol. 3, Issue 9 https://doi.org/10.1101/cshperspect.a009670	journal	June 2011
Dissecting genetic requirements of human breast tumorigenesis in a tissue transgenic model of human breast cancer in mice Wu, Min; Jung, Lina; Cooper, Adrian B. Proceedings of the National Academy of Sciences, Vol. 106, Issue 17 https://doi.org/10.1073/pnas.0811785106	journal	April 2009
Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells Elenbaas, B. Genes & Development, Vol. 15, Issue 1 https://doi.org/10.1101/gad.828901	journal	January 2001
Optimized large-scale production of high titer lentivirus vector pseudotypes Sena-Esteves, Miguel; Tebbets, Jessica C.; Steffens, Sabine Journal of Virological Methods, Vol. 122, Issue 2 https://doi.org/10.1016/j.jviromet.2004.08.017	journal	December 2004
Large-Scale Production of Pseudotyped Lentiviral Vectors Using Baculovirus GP64 Kumar, Mukesh; Bradow, Brian P.; Zimmerberg, Joshua Human Gene Therapy, Vol. 14, Issue 1 https://doi.org/10.1089/10430340360464723	journal	January 2003
Intrinsic Breast Tumor Subtypes, Race, and Long-Term Survival in the Carolina Breast Cancer Study O'Brien, K. M.; Cole, S. R.; Tse, C. -K. Clinical Cancer Research, Vol. 16, Issue 24 https://doi.org/10.1158/1078-0432.CCR-10-1533	journal	December 2010
Lentiviral Transduction of Mammary Stem Cells for Analysis of Gene Function during Development and Cancer Welm, Bryan E.; Dijkgraaf, Gerrit J. P.; Bledau, Anita S. Cell Stem Cell, Vol. 2, Issue 1 https://doi.org/10.1016/j.stem.2007.10.002	journal	January 2008
Clinical and Biological Implications of the Tumor Microenvironment Tarin, David Cancer Microenvironment, Vol. 5, Issue 2 https://doi.org/10.1007/s12307-012-0099-6	journal	February 2012
The morphologies of breast cancer cell lines in three-dimensional assays correlate with their profiles of gene expression Kenny, Paraic A.; Lee, Genee Y.; Myers, Connie A. Molecular Oncology, Vol. 1, Issue 1 https://doi.org/10.1016/j.molonc.2007.02.004	journal	March 2007
A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes Neve, Richard M.; Chin, Koei; Fridlyand, Jane Cancer Cell, Vol. 10, Issue 6 https://doi.org/10.1016/j.ccr.2006.10.008	journal	December 2006
Unraveling the Mechanisms of Endocrine Resistance in Breast Cancer: New Therapeutic Opportunities Massarweh, S.; Schiff, R. Clinical Cancer Research, Vol. 13, Issue 7 https://doi.org/10.1158/1078-0432.ccr-06-2540	journal	April 2007
Sorting Out the FACS: A Devil in the Details Hines, William C.; Su, Ying; Kuhn, Irene Cell Reports, Vol. 6, Issue 5 https://doi.org/10.1016/j.celrep.2014.02.021	journal	March 2014
Modelling breast cancer: one size does not fit all Vargo-Gogola, Tracy; Rosen, Jeffrey M. Nature Reviews Cancer, Vol. 7, Issue 9 https://doi.org/10.1038/nrc2193	journal	September 2007
Stem Cells in the Human Breast Petersen, O. W.; Polyak, K. Cold Spring Harbor Perspectives in Biology, Vol. 2, Issue 5 https://doi.org/10.1101/cshperspect.a003160	journal	May 2010
Creation of human tumour cells with defined genetic elements Hahn, William C.; Counter, Christopher M.; Lundberg, Ante S. Nature, Vol. 400, Issue 6743 https://doi.org/10.1038/22780	journal	July 1999
Analyses of MYC , ERBB2 , and CCND1 Genes in Benign and Malignant Thyroid Follicular Cell Tumors by Real-Time Polymerase Chain Reaction Bièche, Ivan; Franc, Brigitte; Vidaud, Dominique Thyroid, Vol. 11, Issue 2 https://doi.org/10.1089/105072501300042802	journal	February 2001
Molecular portraits of human breast tumours Perou, Charles M.; Sørlie, Therese; Eisen, Michael B. Nature, Vol. 406, Issue 6797 https://doi.org/10.1038/35021093	journal	August 2000
Human Mammary Luminal Epithelial Cells Contain Progenitors to Myoepithelial Cells Péchoux, Christine; Gudjonsson, Thorarinn; Rønnov-Jessen, Lone Developmental Biology, Vol. 206, Issue 1 https://doi.org/10.1006/dbio.1998.9133	journal	February 1999
Defining the cellular precursors to human breast cancer Keller, P. J.; Arendt, L. M.; Skibinski, A. Proceedings of the National Academy of Sciences, Vol. 109, Issue 8 https://doi.org/10.1073/pnas.1017626108	journal	September 2011
ER-to-Golgi transport visualized in living cells Presley, John F.; Cole, Nelson B.; Schroer, Trina A. Nature, Vol. 389, Issue 6646 https://doi.org/10.1038/38001	journal	September 1997
Human mammary epithelial cell transformation through the activation of phosphatidylinositol 3-kinase Zhao, Jean J.; Gjoerup, Ole V.; Subramanian, Romesh R. Cancer Cell, Vol. 3, Issue 5 https://doi.org/10.1016/s1535-6108(03)00088-6	journal	May 2003
Efficient immortalization of luminal epithelial cells from human mammary gland by introduction of simian virus 40 large tumor antigen with a recombinant retrovirus. Bartek, J.; Bartkova, J.; Kyprianou, N. Proceedings of the National Academy of Sciences, Vol. 88, Issue 9 https://doi.org/10.1073/pnas.88.9.3520	journal	May 1991
The MCF10 Model of Breast Tumor Progression Puleo, Julieann; Polyak, Kornelia Cancer Research, Vol. 81, Issue 16 https://doi.org/10.1158/0008-5472.can-21-1939	journal	August 2021
Putting tumours in context Bissell, Mina J.; Radisky, Derek Nature Reviews Cancer, Vol. 1, Issue 1 https://doi.org/10.1038/35094059	journal	October 2001
Transformation of Different Human Breast Epithelial Cell Types Leads to Distinct Tumor Phenotypes Ince, Tan A.; Richardson, Andrea L.; Bell, George W. Cancer Cell, Vol. 12, Issue 2 https://doi.org/10.1016/j.ccr.2007.06.013	journal	August 2007
Molecular Distinctions between Stasis and Telomere Attrition Senescence Barriers Shown by Long-term Culture of Normal Human Mammary Epithelial Cells Garbe, J. C.; Bhattacharya, S.; Merchant, B. Cancer Research, Vol. 69, Issue 19 https://doi.org/10.1158/0008-5472.CAN-09-0270	journal	September 2009
MUC1 and Other Sialoglycoconjugates Inhibit Adenovirus-mediated Gene Transfer to Epithelial Cells Arcasoy, Selim M.; Latoche, Joseph; Gondor, Magdalen American Journal of Respiratory Cell and Molecular Biology, Vol. 17, Issue 4 https://doi.org/10.1165/ajrcmb.17.4.2714	journal	October 1997
Toward a Better Understanding of Race and Cancer Brawley, Otis W. Clinical Cancer Research, Vol. 16, Issue 24 https://doi.org/10.1158/1078-0432.ccr-10-2541	journal	December 2010
Inhibition of adhesion of S-fimbriated Escherichia coli to buccal epithelial cells by human milk fat globule membrane components: a novel aspect of the protective function of mucins in the nonimmunoglobulin fraction. Schroten, H.; Hanisch, F. G.; Plogmann, R. Infection and Immunity, Vol. 60, Issue 7 https://doi.org/10.1128/iai.60.7.2893-2899.1992	journal	January 1992
Serum-free growth of human mammary epithelial cells: rapid clonal growth in defined medium and extended serial passage with pituitary extract. Hammond, S. L.; Ham, R. G.; Stampfer, M. R. Proceedings of the National Academy of Sciences, Vol. 81, Issue 17 https://doi.org/10.1073/pnas.81.17.5435	journal	September 1984
High-efficiency gene transfer into CD34+ cells with a human immunodeficiency virus type 1-based retroviral vector pseudotyped with vesicular stomatitis virus envelope glycoprotein G. Akkina, R. K.; Walton, R. M.; Chen, M. L. Journal of virology, Vol. 70, Issue 4 https://doi.org/10.1128/jvi.70.4.2581-2585.1996	journal	January 1996
Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression Bissell, Mina J.; Hines, William C. Nature Medicine, Vol. 17, Issue 3 https://doi.org/10.1038/nm.2328	journal	March 2011
Mammary epithelial cell transformation: insights from cell culture and mouse models Dimri, Goberdhan; Band, Hamid; Band, Vimla Breast Cancer Research, Vol. 7, Issue 4 https://doi.org/10.1186/bcr1275	journal	June 2005
Phosphatidylserine Is Not the Cell Surface Receptor for Vesicular Stomatitis Virus Coil, D. A.; Miller, A. D. Journal of Virology, Vol. 78, Issue 20 https://doi.org/10.1128/jvi.78.20.10920-10926.2004	journal	September 2004
Choosing the right cell line for breast cancer research Holliday, Deborah L.; Speirs, Valerie Breast Cancer Research, Vol. 13, Issue 4 https://doi.org/10.1186/bcr2889	journal	August 2011
Self-Inactivating Lentivirus Vector for Safe and Efficient In Vivo Gene Delivery Zufferey, Romain; Dull, Thomas; Mandel, Ronald J. Journal of Virology, Vol. 72, Issue 12 https://doi.org/10.1128/JVI.72.12.9873-9880.1998	journal	December 1998
Covalent Modifications of the Ebola Virus Glycoprotein Jeffers, S. A.; Sanders, D. A.; Sanchez, A. Journal of Virology, Vol. 76, Issue 24 https://doi.org/10.1128/jvi.76.24.12463-12472.2002	journal	December 2002
A new diploid nontumorigenic human breast epithelial cell line isolated and propagated in chemically defined medium Briand, P.; Petersen, O. W.; Deurs, B. In Vitro Cellular & Developmental Biology, Vol. 23, Issue 3 https://doi.org/10.1007/bf02623578	journal	March 1987
Keratin expression in human mammary epithelial cells cultured from normal and malignant tissue: relation to in vivo phenotypes and influence of medium Taylor-Papadimitriou, J.; Stampfer, M.; Barter, J. Journal of Cell Science, Vol. 94, Issue 3 https://doi.org/10.1242/jcs.94.3.403	journal	November 1989

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Oncogenic HrasG12V expression plus knockdown of Cdkn2a using ecotropic lentiviral vectors induces high-grade endometrial stromal sarcoma Brandt, Laura P.; Albers, Joachim; Hejhal, Tomas PLOS ONE, Vol. 12, Issue 10 https://doi.org/10.1371/journal.pone.0186102	journal	October 2017
Isolation of Mouse and Human Tumor-Associated Macrophages Cassetta, Luca; Noy, Roy; Swierczak, Agnieszka Tumor Microenvironment https://doi.org/10.1007/978-3-319-26666-4_12	book	January 2016
A 3D in vitro model of the human breast duct: a method to unravel myoepithelial-luminal interactions in the progression of breast cancer Carter, Edward P.; Gopsill, James A.; Gomm, Jennifer. J. Breast Cancer Research, Vol. 19, Issue 1 https://doi.org/10.1186/s13058-017-0843-4	journal	April 2017
Transformation of enriched mammary cell populations with polyomavirus middle T antigen influences tumor subtype and metastatic potential Drobysheva, Daria; Smith, Brittni Alise; McDowell, Maria Breast Cancer Research, Vol. 17, Issue 1 https://doi.org/10.1186/s13058-015-0641-9	journal	October 2015
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Propagation of oestrogen receptor-positive and oestrogen-responsive normal human breast cells in culture Fridriksdottir, Agla J.; Kim, Jiyoung; Villadsen, René Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9786	journal	November 2015

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