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[Preprint]. 2023 Sep 17:2023.09.15.557802. [Version 1] doi: 10.1101/2023.09.15.557802

Trogocytosis of cancer-associated fibroblasts promotes pancreatic cancer growth and immune suppression via phospholipid scramblase anoctamin 6 (ANO6)

Charline Ogier, Akino Mercy Charles Solomon, Zhen Lu, Ludmila Recoules, Alena Klochkova, Linara Gabitova-Cornell, Battuya Bayarmagnai, Diana Restifo, Aizhan Surumbayeva, Débora B Vendramini-Costa, Alexander Y Deneka, Ralph Francescone, Anna C Lilly, Alyssa Sipman, Jaye C Gardiner, Tiffany Luong, Janusz Franco-Barraza, Nina Ibeme, Kathy Q Cai, Margret B Einarson, Emmanuelle Nicolas, Andrei Efimov, Emily Megill, Nathaniel W Snyder, Corinne Bousquet, Jerome Cros, Yunyun Zhou, Erica A Golemis, Bojana Gligorijevic, Jonathan Soboloff, Serge Y Fuchs, Edna Cukierman, Igor Astsaturov
PMCID: PMC10515956  PMID: 37745612

Abstract

In pancreatic ductal adenocarcinoma (PDAC), the fibroblastic stroma constitutes most of the tumor mass and is remarkably devoid of functional blood vessels. This raises an unresolved question of how PDAC cells obtain essential metabolites and water-insoluble lipids. We have found a critical role for cancer-associated fibroblasts (CAFs) in obtaining and transferring lipids from blood-borne particles to PDAC cells via trogocytosis of CAF plasma membranes. We have also determined that CAF-expressed phospholipid scramblase anoctamin 6 (ANO6) is an essential CAF trogocytosis regulator required to promote PDAC cell survival. During trogocytosis, cancer cells and CAFs form synapse-like plasma membranes contacts that induce cytosolic calcium influx in CAFs via Orai channels. This influx activates ANO6 and results in phosphatidylserine exposure on CAF plasma membrane initiating trogocytosis and transfer of membrane lipids, including cholesterol, to PDAC cells. Importantly, ANO6-dependent trogocytosis also supports the immunosuppressive function of pancreatic CAFs towards cytotoxic T cells by promoting transfer of excessive amounts of cholesterol. Further, blockade of ANO6 antagonizes tumor growth via disruption of delivery of exogenous cholesterol to cancer cells and reverses immune suppression suggesting a potential new strategy for PDAC therapy.

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