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 language | English (US) |
|---|---|
| Pages (from-to) | 549-562.e6 |
| Journal | Developmental Cell |
| Volume | 43 |
| Issue number | 5 |
| DOIs | |
| State | Published - Dec 4 2017 |
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Keywords
- cell migration
- contact-dependent cell communication
- cytoplasmic transfer
- macrophages
- melanoma
- mouse
- tumor microenvironment
- zebrafish
ASJC Scopus subject areas
- Developmental Biology
Cite this
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 H.; Condeelis, John S.; Moens, Cecilia B.
In: Developmental Cell, Vol. 43, No. 5, 04.12.2017, p. 549-562.e6.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - Macrophage-Dependent Cytoplasmic Transfer during Melanoma Invasion In Vivo
AU - Roh-Johnson, Minna
AU - Shah, Arish N.
AU - Stonick, Jason A.
AU - Poudel, Kumud R.
AU - Kargl, Julia
AU - Yang, Grace H.
AU - di Martino, Julie
AU - Hernandez, Rafael E.
AU - Gast, Charles E.
AU - Zarour, Luai R.
AU - Antoku, Susumu
AU - Houghton, A. Mc Garry
AU - Bravo-Cordero, Jose Javier
AU - Wong, Melissa H.
AU - Condeelis, John S.
AU - Moens, Cecilia B.
PY - 2017/12/4
Y1 - 2017/12/4
N2 - 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.
AB - 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.
KW - cell migration
KW - contact-dependent cell communication
KW - cytoplasmic transfer
KW - macrophages
KW - melanoma
KW - mouse
KW - tumor microenvironment
KW - zebrafish
UR - http://www.scopus.com/inward/record.url?scp=85035346492&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85035346492&partnerID=8YFLogxK
U2 - 10.1016/j.devcel.2017.11.003
DO - 10.1016/j.devcel.2017.11.003
M3 - Article
C2 - 29207258
AN - SCOPUS:85035346492
VL - 43
SP - 549-562.e6
JO - Developmental Cell
JF - Developmental Cell
SN - 1534-5807
IS - 5
ER -