Primary tumor associated macrophages activate programs of invasion and dormancy in disseminating tumor cells

Lucia Borriello, Anouchka Coste, Brian Traub, Ved P. Sharma, George S. Karagiannis, Yu Lin, Yarong Wang, Xianjun Ye, Camille L. Duran, Xiaoming Chen, Madeline Friedman, Maria Soledad Sosa, Dan Sun, Erica Dalla, Deepak K. Singh, Maja H. Oktay, Julio A. Aguirre-Ghiso (), John S. Condeelis () and David Entenberg ()
Additional contact information
Lucia Borriello: Albert Einstein College of Medicine/Montefiore Medical Center
Anouchka Coste: Albert Einstein College of Medicine/Montefiore Medical Center
Brian Traub: Albert Einstein College of Medicine/Montefiore Medical Center
Ved P. Sharma: Albert Einstein College of Medicine/Montefiore Medical Center
George S. Karagiannis: Albert Einstein College of Medicine/Montefiore Medical Center
Yu Lin: Albert Einstein College of Medicine/Montefiore Medical Center
Yarong Wang: Albert Einstein College of Medicine/Montefiore Medical Center
Xianjun Ye: Albert Einstein College of Medicine/Montefiore Medical Center
Camille L. Duran: Albert Einstein College of Medicine/Montefiore Medical Center
Xiaoming Chen: Albert Einstein College of Medicine/Montefiore Medical Center
Madeline Friedman: Albert Einstein College of Medicine/Montefiore Medical Center
Maria Soledad Sosa: Icahn School of Medicine at Mount Sinai
Dan Sun: Albert Einstein College of Medicine/Montefiore Medical Center
Erica Dalla: Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai
Deepak K. Singh: Albert Einstein College of Medicine/Montefiore Medical Center
Maja H. Oktay: Albert Einstein College of Medicine/Montefiore Medical Center
Julio A. Aguirre-Ghiso: Albert Einstein College of Medicine/Montefiore Medical Center
John S. Condeelis: Albert Einstein College of Medicine/Montefiore Medical Center
David Entenberg: Albert Einstein College of Medicine/Montefiore Medical Center

Nature Communications, 2022, vol. 13, issue 1, 1-19

Abstract: Abstract Metastases are initiated by disseminated tumor cells (DTCs) that colonize distant organs. Growing evidence suggests that the microenvironment of the primary tumor primes DTCs for dormant or proliferative fates. However, the manner in which this occurs remains poorly understood. Here, using the Window for High-Resolution Intravital Imaging of the Lung (WHRIL), we study the live lung longitudinally and follow the fate of individual DTCs that spontaneously disseminate from orthotopic breast tumors. We find that spontaneously DTCs have increased levels of retention, increased speed of extravasation, and greater survival after extravasation, compared to experimentally metastasized tumor cells. Detailed analysis reveals that a subset of macrophages within the primary tumor induces a pro-dissemination and pro-dormancy DTC phenotype. Our work provides insight into how specific primary tumor microenvironments prime a subpopulation of cells for expression of proteins associated with dissemination and dormancy.

Date: 2022
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DOI: 10.1038/s41467-022-28076-3

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