Hormonal regulation of epithelial organization in a three-dimensional breast tissue culture model.

Lucia Speroni, Gregory S Whitt, Joanna Xylas, Kyle P Quinn, Adeline Jondeau-Cabaton, Clifford Barnes, Irene Georgakoudi, Carlos Sonnenschein, Ana M Soto

    Research output: Contribution to journalArticle

    Abstract

    The establishment of hormone target breast cells in the 1970's resulted in suitable models for the study of hormone control of cell proliferation and gene expression using two-dimensional (2D) cultures. However, in order to study mammogenesis and breast tumor development in vitro, cells must be able to organize in three-dimensional (3D) structures like in the tissue. We now report the development of a hormone- sensitive three-dimensional (3D) culture model for the study of mammogenesis and neoplastic development. Hormone-sensitive T47D breast cancer cells respond to estradiol in a dose dependent manner by forming complex epithelial structures. Treatment with the synthetic progestagen promegestone, in the presence of estradiol, results in flat epithelial structures that display cytoplasmic projections, a phenomenon reported to precede side-branching. Additionally, as in the mammary gland, treatment with prolactin in the presence of estradiol induces budding structures. These changes in epithelial organization are accompanied by collagen remodeling. Collagen is the major acellular component of the breast stroma and an important player in tumor development and progression. Quantitative analysis of second harmonic generation of collagen fibers revealed that collagen density was more variable surrounding budding and irregularly shaped structures when compared to more regular structures; suggesting that fiber organization in the former is more anisotropic than in the latter. In sum, this new 3D model recapitulates morphogenetic events modulated by mammogenic hormones in the breast, and is suitable for the evaluation of therapeutic agents.
    LanguageEnglish
    JournalTissue Engineering Part C Methods
    Volumepart c
    DOIs
    Publication statusPublished - 2013

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    Tissue culture
    Hormones
    Breast
    Collagen
    Estradiol
    Tumors
    Promegestone
    Progesterone Congeners
    Cytoplasmic Structures
    Breast Neoplasms
    Fibers
    Cell proliferation
    Human Mammary Glands
    Harmonic generation
    Gene expression
    Prolactin
    Cells
    Cell Proliferation
    Tissue
    Gene Expression

    Cite this

    Speroni, L., Whitt, G. S., Xylas, J., Quinn, K. P., Jondeau-Cabaton, A., Barnes, C., ... Soto, A. M. (2013). Hormonal regulation of epithelial organization in a three-dimensional breast tissue culture model. part c. https://doi.org/10.1089/ten.TEC.2013.0054.
    Speroni, Lucia ; Whitt, Gregory S ; Xylas, Joanna ; Quinn, Kyle P ; Jondeau-Cabaton, Adeline ; Barnes, Clifford ; Georgakoudi, Irene ; Sonnenschein, Carlos ; Soto, Ana M. / Hormonal regulation of epithelial organization in a three-dimensional breast tissue culture model. 2013 ; Vol. part c.
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    abstract = "The establishment of hormone target breast cells in the 1970's resulted in suitable models for the study of hormone control of cell proliferation and gene expression using two-dimensional (2D) cultures. However, in order to study mammogenesis and breast tumor development in vitro, cells must be able to organize in three-dimensional (3D) structures like in the tissue. We now report the development of a hormone- sensitive three-dimensional (3D) culture model for the study of mammogenesis and neoplastic development. Hormone-sensitive T47D breast cancer cells respond to estradiol in a dose dependent manner by forming complex epithelial structures. Treatment with the synthetic progestagen promegestone, in the presence of estradiol, results in flat epithelial structures that display cytoplasmic projections, a phenomenon reported to precede side-branching. Additionally, as in the mammary gland, treatment with prolactin in the presence of estradiol induces budding structures. These changes in epithelial organization are accompanied by collagen remodeling. Collagen is the major acellular component of the breast stroma and an important player in tumor development and progression. Quantitative analysis of second harmonic generation of collagen fibers revealed that collagen density was more variable surrounding budding and irregularly shaped structures when compared to more regular structures; suggesting that fiber organization in the former is more anisotropic than in the latter. In sum, this new 3D model recapitulates morphogenetic events modulated by mammogenic hormones in the breast, and is suitable for the evaluation of therapeutic agents.",
    author = "Lucia Speroni and Whitt, {Gregory S} and Joanna Xylas and Quinn, {Kyle P} and Adeline Jondeau-Cabaton and Clifford Barnes and Irene Georgakoudi and Carlos Sonnenschein and Soto, {Ana M}",
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    Speroni, L, Whitt, GS, Xylas, J, Quinn, KP, Jondeau-Cabaton, A, Barnes, C, Georgakoudi, I, Sonnenschein, C & Soto, AM 2013, 'Hormonal regulation of epithelial organization in a three-dimensional breast tissue culture model.', vol. part c. https://doi.org/10.1089/ten.TEC.2013.0054.

    Hormonal regulation of epithelial organization in a three-dimensional breast tissue culture model. / Speroni, Lucia; Whitt, Gregory S; Xylas, Joanna; Quinn, Kyle P; Jondeau-Cabaton, Adeline; Barnes, Clifford; Georgakoudi, Irene; Sonnenschein, Carlos; Soto, Ana M.

    Vol. part c, 2013.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Hormonal regulation of epithelial organization in a three-dimensional breast tissue culture model.

    AU - Speroni, Lucia

    AU - Whitt, Gregory S

    AU - Xylas, Joanna

    AU - Quinn, Kyle P

    AU - Jondeau-Cabaton, Adeline

    AU - Barnes, Clifford

    AU - Georgakoudi, Irene

    AU - Sonnenschein, Carlos

    AU - Soto, Ana M

    PY - 2013

    Y1 - 2013

    N2 - The establishment of hormone target breast cells in the 1970's resulted in suitable models for the study of hormone control of cell proliferation and gene expression using two-dimensional (2D) cultures. However, in order to study mammogenesis and breast tumor development in vitro, cells must be able to organize in three-dimensional (3D) structures like in the tissue. We now report the development of a hormone- sensitive three-dimensional (3D) culture model for the study of mammogenesis and neoplastic development. Hormone-sensitive T47D breast cancer cells respond to estradiol in a dose dependent manner by forming complex epithelial structures. Treatment with the synthetic progestagen promegestone, in the presence of estradiol, results in flat epithelial structures that display cytoplasmic projections, a phenomenon reported to precede side-branching. Additionally, as in the mammary gland, treatment with prolactin in the presence of estradiol induces budding structures. These changes in epithelial organization are accompanied by collagen remodeling. Collagen is the major acellular component of the breast stroma and an important player in tumor development and progression. Quantitative analysis of second harmonic generation of collagen fibers revealed that collagen density was more variable surrounding budding and irregularly shaped structures when compared to more regular structures; suggesting that fiber organization in the former is more anisotropic than in the latter. In sum, this new 3D model recapitulates morphogenetic events modulated by mammogenic hormones in the breast, and is suitable for the evaluation of therapeutic agents.

    AB - The establishment of hormone target breast cells in the 1970's resulted in suitable models for the study of hormone control of cell proliferation and gene expression using two-dimensional (2D) cultures. However, in order to study mammogenesis and breast tumor development in vitro, cells must be able to organize in three-dimensional (3D) structures like in the tissue. We now report the development of a hormone- sensitive three-dimensional (3D) culture model for the study of mammogenesis and neoplastic development. Hormone-sensitive T47D breast cancer cells respond to estradiol in a dose dependent manner by forming complex epithelial structures. Treatment with the synthetic progestagen promegestone, in the presence of estradiol, results in flat epithelial structures that display cytoplasmic projections, a phenomenon reported to precede side-branching. Additionally, as in the mammary gland, treatment with prolactin in the presence of estradiol induces budding structures. These changes in epithelial organization are accompanied by collagen remodeling. Collagen is the major acellular component of the breast stroma and an important player in tumor development and progression. Quantitative analysis of second harmonic generation of collagen fibers revealed that collagen density was more variable surrounding budding and irregularly shaped structures when compared to more regular structures; suggesting that fiber organization in the former is more anisotropic than in the latter. In sum, this new 3D model recapitulates morphogenetic events modulated by mammogenic hormones in the breast, and is suitable for the evaluation of therapeutic agents.

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