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Cancer-associated fibroblasts reuse cancer-derived lactate to maintain a fibrotic and immunosuppressive microenvironment in pancreatic cancer

Glycolysis is highly enhanced in pancreatic ductal adenocarcinoma (PDAC) cells; thus, glucose restrictions are imposed on nontumor cells in the PDAC tumor microenvironment (TME). However, little is known about how such glucose competition alters metabolism and confers phenotypic changes in stromal c...

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Autores principales: Kitamura, Fumimasa, Semba, Takashi, Yasuda-Yoshihara, Noriko, Yamada, Kosuke, Nishimura, Akiho, Yamasaki, Juntaro, Nagano, Osamu, Yasuda, Tadahito, Yonemura, Atsuko, Tong, Yilin, Wang, Huaitao, Akiyama, Takahiko, Matsumura, Kazuki, Uemura, Norio, Itoyama, Rumi, Bu, Luke, Fu, Lingfeng, Hu, Xichen, Wei, Feng, Mima, Kosuke, Imai, Katsunori, Hayashi, Hiromitsu, Yamashita, Yo-ichi, Miyamoto, Yuji, Baba, Hideo, Ishimoto, Takatsugu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Clinical Investigation 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619496/
https://www.ncbi.nlm.nih.gov/pubmed/37733442
http://dx.doi.org/10.1172/jci.insight.163022
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author Kitamura, Fumimasa
Semba, Takashi
Yasuda-Yoshihara, Noriko
Yamada, Kosuke
Nishimura, Akiho
Yamasaki, Juntaro
Nagano, Osamu
Yasuda, Tadahito
Yonemura, Atsuko
Tong, Yilin
Wang, Huaitao
Akiyama, Takahiko
Matsumura, Kazuki
Uemura, Norio
Itoyama, Rumi
Bu, Luke
Fu, Lingfeng
Hu, Xichen
Wei, Feng
Mima, Kosuke
Imai, Katsunori
Hayashi, Hiromitsu
Yamashita, Yo-ichi
Miyamoto, Yuji
Baba, Hideo
Ishimoto, Takatsugu
author_facet Kitamura, Fumimasa
Semba, Takashi
Yasuda-Yoshihara, Noriko
Yamada, Kosuke
Nishimura, Akiho
Yamasaki, Juntaro
Nagano, Osamu
Yasuda, Tadahito
Yonemura, Atsuko
Tong, Yilin
Wang, Huaitao
Akiyama, Takahiko
Matsumura, Kazuki
Uemura, Norio
Itoyama, Rumi
Bu, Luke
Fu, Lingfeng
Hu, Xichen
Wei, Feng
Mima, Kosuke
Imai, Katsunori
Hayashi, Hiromitsu
Yamashita, Yo-ichi
Miyamoto, Yuji
Baba, Hideo
Ishimoto, Takatsugu
author_sort Kitamura, Fumimasa
collection PubMed
description Glycolysis is highly enhanced in pancreatic ductal adenocarcinoma (PDAC) cells; thus, glucose restrictions are imposed on nontumor cells in the PDAC tumor microenvironment (TME). However, little is known about how such glucose competition alters metabolism and confers phenotypic changes in stromal cells in the TME. Here, we report that cancer-associated fibroblasts (CAFs) with restricted glucose availability utilize lactate from glycolysis-enhanced cancer cells as a fuel and exert immunosuppressive activity in the PDAC TME. The expression of lactate dehydrogenase A (LDHA), which regulates lactate production, was a poor prognostic factor for patients with PDAC, and LDHA depletion suppressed tumor growth in a CAF-rich murine PDAC model. Coculture of CAFs with PDAC cells revealed that most of the glucose was taken up by the tumor cells and that CAFs consumed lactate via monocarboxylate transporter 1 to enhance proliferation through the TCA cycle. Moreover, lactate-stimulated CAFs upregulated IL-6 expression and suppressed cytotoxic immune cell activity synergistically with lactate. Finally, the LDHA inhibitor FX11 reduced tumor growth and improved antitumor immunity in CAF-rich PDAC tumors. Our study provides insight regarding the crosstalk among tumor cells, CAFs, and immune cells mediated by lactate and offers therapeutic strategies for targeting LDHA enzymatic activity in PDAC cells.
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spelling pubmed-106194962023-11-02 Cancer-associated fibroblasts reuse cancer-derived lactate to maintain a fibrotic and immunosuppressive microenvironment in pancreatic cancer Kitamura, Fumimasa Semba, Takashi Yasuda-Yoshihara, Noriko Yamada, Kosuke Nishimura, Akiho Yamasaki, Juntaro Nagano, Osamu Yasuda, Tadahito Yonemura, Atsuko Tong, Yilin Wang, Huaitao Akiyama, Takahiko Matsumura, Kazuki Uemura, Norio Itoyama, Rumi Bu, Luke Fu, Lingfeng Hu, Xichen Wei, Feng Mima, Kosuke Imai, Katsunori Hayashi, Hiromitsu Yamashita, Yo-ichi Miyamoto, Yuji Baba, Hideo Ishimoto, Takatsugu JCI Insight Research Article Glycolysis is highly enhanced in pancreatic ductal adenocarcinoma (PDAC) cells; thus, glucose restrictions are imposed on nontumor cells in the PDAC tumor microenvironment (TME). However, little is known about how such glucose competition alters metabolism and confers phenotypic changes in stromal cells in the TME. Here, we report that cancer-associated fibroblasts (CAFs) with restricted glucose availability utilize lactate from glycolysis-enhanced cancer cells as a fuel and exert immunosuppressive activity in the PDAC TME. The expression of lactate dehydrogenase A (LDHA), which regulates lactate production, was a poor prognostic factor for patients with PDAC, and LDHA depletion suppressed tumor growth in a CAF-rich murine PDAC model. Coculture of CAFs with PDAC cells revealed that most of the glucose was taken up by the tumor cells and that CAFs consumed lactate via monocarboxylate transporter 1 to enhance proliferation through the TCA cycle. Moreover, lactate-stimulated CAFs upregulated IL-6 expression and suppressed cytotoxic immune cell activity synergistically with lactate. Finally, the LDHA inhibitor FX11 reduced tumor growth and improved antitumor immunity in CAF-rich PDAC tumors. Our study provides insight regarding the crosstalk among tumor cells, CAFs, and immune cells mediated by lactate and offers therapeutic strategies for targeting LDHA enzymatic activity in PDAC cells. American Society for Clinical Investigation 2023-10-23 /pmc/articles/PMC10619496/ /pubmed/37733442 http://dx.doi.org/10.1172/jci.insight.163022 Text en © 2023 Kitamura et al. https://creativecommons.org/licenses/by/4.0/This work is licensed under the Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Kitamura, Fumimasa
Semba, Takashi
Yasuda-Yoshihara, Noriko
Yamada, Kosuke
Nishimura, Akiho
Yamasaki, Juntaro
Nagano, Osamu
Yasuda, Tadahito
Yonemura, Atsuko
Tong, Yilin
Wang, Huaitao
Akiyama, Takahiko
Matsumura, Kazuki
Uemura, Norio
Itoyama, Rumi
Bu, Luke
Fu, Lingfeng
Hu, Xichen
Wei, Feng
Mima, Kosuke
Imai, Katsunori
Hayashi, Hiromitsu
Yamashita, Yo-ichi
Miyamoto, Yuji
Baba, Hideo
Ishimoto, Takatsugu
Cancer-associated fibroblasts reuse cancer-derived lactate to maintain a fibrotic and immunosuppressive microenvironment in pancreatic cancer
title Cancer-associated fibroblasts reuse cancer-derived lactate to maintain a fibrotic and immunosuppressive microenvironment in pancreatic cancer
title_full Cancer-associated fibroblasts reuse cancer-derived lactate to maintain a fibrotic and immunosuppressive microenvironment in pancreatic cancer
title_fullStr Cancer-associated fibroblasts reuse cancer-derived lactate to maintain a fibrotic and immunosuppressive microenvironment in pancreatic cancer
title_full_unstemmed Cancer-associated fibroblasts reuse cancer-derived lactate to maintain a fibrotic and immunosuppressive microenvironment in pancreatic cancer
title_short Cancer-associated fibroblasts reuse cancer-derived lactate to maintain a fibrotic and immunosuppressive microenvironment in pancreatic cancer
title_sort cancer-associated fibroblasts reuse cancer-derived lactate to maintain a fibrotic and immunosuppressive microenvironment in pancreatic cancer
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619496/
https://www.ncbi.nlm.nih.gov/pubmed/37733442
http://dx.doi.org/10.1172/jci.insight.163022
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