Macrophage-Dependent Cytoplasmic Transfer during Melanoma Invasion In Vivo

Minna Roh-Johnson, Arish N. Shah, Jason A. Stonick, Kumud R. Poudel, Julia Kargl, Grace H. Yang, Julie di Martino, Rafael E. Hernandez, Charles E. Gast, Luai R. Zarour, Susumu Antoku, A. Mc Garry Houghton, Jose Javier Bravo-Cordero, Melissa Wong, John Condeelis, Cecilia B. Moens

    Research output: Contribution to journalArticle

    25 Citations (Scopus)

    Abstract

    Interactions between tumor cells and tumor-associated macrophages play critical roles in the initiation of tumor cell motility. To capture the cellular interactions of the tumor microenvironment with high-resolution imaging, we directly visualized tumor cells and their interactions with macrophages in zebrafish. Live imaging in zebrafish revealed that macrophages are dynamic, yet maintain sustained contact with tumor cells. In addition, the recruitment of macrophages to tumor cells promotes tumor cell dissemination. Using a Cre/LoxP strategy, we found that macrophages transfer cytoplasm to tumor cells in zebrafish and mouse models. Remarkably, macrophage cytoplasmic transfer correlated with melanoma cell dissemination. We further found that macrophages transfer cytoplasm to tumor cells upon cell contact in vitro. Thus, we present a model in which macrophage/tumor cell contact allows for the transfer of cytoplasmic molecules from macrophages to tumor cells corresponding to increased tumor cell motility and dissemination. Roh-Johnson et al. show that macrophages transfer cytoplasmic molecules to tumor cells via cell contact in zebrafish and mouse. Cytoplasmic transfer correlates with increased tumor cell dissemination in vivo and altered tumor cell migration in vitro. These results uncover a mode of contact-dependent cell-to-cell communication in the tumor microenvironment.

    Original languageEnglish (US)
    Pages (from-to)549-562.e6
    JournalDevelopmental Cell
    Volume43
    Issue number5
    DOIs
    StatePublished - Dec 4 2017

    Fingerprint

    Macrophages
    Tumors
    Melanoma
    Cells
    Neoplasms
    Zebrafish
    Cell Movement
    Tumor Microenvironment
    Cell Communication
    Cytoplasm
    Imaging techniques
    Molecules

    Keywords

    • cell migration
    • contact-dependent cell communication
    • cytoplasmic transfer
    • macrophages
    • melanoma
    • mouse
    • tumor microenvironment
    • zebrafish

    ASJC Scopus subject areas

    • Developmental Biology

    Cite this

    Roh-Johnson, M., Shah, A. N., Stonick, J. A., Poudel, K. R., Kargl, J., Yang, G. H., ... Moens, C. B. (2017). Macrophage-Dependent Cytoplasmic Transfer during Melanoma Invasion In Vivo. Developmental Cell, 43(5), 549-562.e6. https://doi.org/10.1016/j.devcel.2017.11.003

    Macrophage-Dependent Cytoplasmic Transfer during Melanoma Invasion In Vivo. / Roh-Johnson, Minna; Shah, Arish N.; Stonick, Jason A.; Poudel, Kumud R.; Kargl, Julia; Yang, Grace H.; di Martino, Julie; Hernandez, Rafael E.; Gast, Charles E.; Zarour, Luai R.; Antoku, Susumu; Houghton, A. Mc Garry; Bravo-Cordero, Jose Javier; Wong, Melissa; Condeelis, John; Moens, Cecilia B.

    In: Developmental Cell, Vol. 43, No. 5, 04.12.2017, p. 549-562.e6.

    Research output: Contribution to journalArticle

    Roh-Johnson, M, Shah, AN, Stonick, JA, Poudel, KR, Kargl, J, Yang, GH, di Martino, J, Hernandez, RE, Gast, CE, Zarour, LR, Antoku, S, Houghton, AMG, Bravo-Cordero, JJ, Wong, M, Condeelis, J & Moens, CB 2017, 'Macrophage-Dependent Cytoplasmic Transfer during Melanoma Invasion In Vivo', Developmental Cell, vol. 43, no. 5, pp. 549-562.e6. https://doi.org/10.1016/j.devcel.2017.11.003
    Roh-Johnson M, Shah AN, Stonick JA, Poudel KR, Kargl J, Yang GH et al. Macrophage-Dependent Cytoplasmic Transfer during Melanoma Invasion In Vivo. Developmental Cell. 2017 Dec 4;43(5):549-562.e6. https://doi.org/10.1016/j.devcel.2017.11.003
    Roh-Johnson, Minna ; Shah, Arish N. ; Stonick, Jason A. ; Poudel, Kumud R. ; Kargl, Julia ; Yang, Grace H. ; di Martino, Julie ; Hernandez, Rafael E. ; Gast, Charles E. ; Zarour, Luai R. ; Antoku, Susumu ; Houghton, A. Mc Garry ; Bravo-Cordero, Jose Javier ; Wong, Melissa ; Condeelis, John ; Moens, Cecilia B. / Macrophage-Dependent Cytoplasmic Transfer during Melanoma Invasion In Vivo. In: Developmental Cell. 2017 ; Vol. 43, No. 5. pp. 549-562.e6.
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