Neoadjuvant Chemotherapy Induces IL34 Signaling and Promotes Chemoresistance via Tumor-Associated Macrophage Polarization in Esophageal Squamous Cell Carcinoma.


Journal

Molecular cancer research : MCR
ISSN: 1557-3125
Titre abrégé: Mol Cancer Res
Pays: United States
ID NLM: 101150042

Informations de publication

Date de publication:
06 2021
Historique:
received: 15 10 2020
revised: 26 01 2021
accepted: 02 03 2021
pubmed: 7 3 2021
medline: 27 1 2022
entrez: 6 3 2021
Statut: ppublish

Résumé

The tumor microenvironment (TME) plays a key role in the efficacy of neoadjuvant chemotherapy (NAC) in solid tumors including esophageal squamous cell carcinoma (ESCC). However, the TME profile of ESCC treated with NAC is not fully understood. In this study, we investigated the effect of NAC on the TME especially tumor-associated macrophages (TAM), the important immunosuppressive components of the TME, in ESCC. We quantified the expression of CD163, a crucial marker of TAM, in pretherapeutic biopsy and surgically resected ESCC specimens from patients who received NAC (

Identifiants

pubmed: 33674443
pii: 1541-7786.MCR-20-0917
doi: 10.1158/1541-7786.MCR-20-0917
doi:

Substances chimiques

Antigens, CD 0
Antigens, Differentiation, Myelomonocytic 0
CD163 antigen 0
IL34 protein, human 0
Interleukins 0
Receptors, Cell Surface 0
Cisplatin Q20Q21Q62J
Fluorouracil U3P01618RT

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1085-1095

Informations de copyright

©2021 American Association for Cancer Research.

Références

Enzinger PC, Mayer RJ. Esophageal cancer. N Engl J Med. 2003;349:2241–52.
Ando N, Kato H, Igaki H, Shinoda M, Ozawa S, Shimizu H, et al. A randomized trial comparing postoperative adjuvant chemotherapy with cisplatin and 5-fluorouracil versus preoperative chemotherapy for localized advanced squamous cell carcinoma of the thoracic esophagus (JCOG9907). Ann Surg Oncol. 2012;19:68–74.
Mantovani A, Marchesi F, Malesci A, Laghi L, Allavena P. Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol. 2017;14:399–416.
Barros MH, Hauck F, Dreyer JH, Kempkes B, Niedobitek G. Macrophage polarisation: an immunohistochemical approach for identifying M1 and M2 macrophages. PLoS One. 2013;8:e80908.
Aras S, Zaidi MR. TAMeless traitors: macrophages in cancer progression and metastasis. Br J Cancer. 2017;117:1583–91.
Chen Y, Song Y, Du W, Gong L, Chang H, Zou Z. Tumor-associated macrophages: an accomplice in solid tumor progression. J Biomed Sci. 2019;26:78.
Yagi T, Baba Y, Okadome K, Kiyozumi Y, Hiyoshi Y, Ishimoto T, et al. Tumour-associated macrophages are associated with poor prognosis and programmed death ligand 1 expression in oesophageal cancer. Eur J Cancer. 2019;111:38–49.
Koide N, Nishio A, Hiraguri M, Kishimoto K, Nakamura T, Adachi W, et al. Differences and relationships of thymidine phosphorylase expression in tumor-associated macrophages and cancer cells in squamous cell carcinoma of the esophagus. Dis Esophagus. 2002;15:67–73.
Xu B, Chen L, Li J, Zheng X, Shi L, Wu C, et al. Prognostic value of tumor infiltrating NK cells and macrophages in stage II+III esophageal cancer patients. Oncotarget. 2016;7:74904–16.
Li J, Xie Y, Wang X, Li F, Li S, Li M, et al. Prognostic impact of tumor-associated macrophage infiltration in esophageal cancer: a meta-analysis. Future Oncol. 2019;15:2303–17.
Sugimura K, Miyata H, Tanaka K, Takahashi T, Kurokawa Y, Yamasaki M, et al. High infiltration of tumor-associated macrophages is associated with a poor response to chemotherapy and poor prognosis of patients undergoing neoadjuvant chemotherapy for esophageal cancer. J Surg Oncol. 2015;111:752–9.
Yamamoto K, Makino T, Sato E, Noma T, Urakawa S, Takeoka T, et al. Tumor-infiltrating M2 macrophage in pretreatment biopsy sample predicts response to chemotherapy and survival in esophageal cancer. Cancer Sci. 2020;111:1103–12.
Stanley ER, Chen DM, Lin HS. Induction of macrophage production and proliferation by a purified colony stimulating factor. Nature. 1978;274:168–70.
Lin EY, Nguyen AV, Russell RG, Pollard JW. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med. 2001;193:727–40.
Curry JM, Eubank TD, Roberts RD, Wang Y, Pore N, Maity A, et al. M-CSF signals through the MAPK/ERK pathway via Sp1 to induce VEGF production and induces angiogenesis in vivo. PLoS One. 2008;3:e3405.
Scholl SM, Pallud C, Beuvon F, Hacene K, Stanley ER, Rohrschneider L, et al. Anti-colony-stimulating factor-1 antibody staining in primary breast adenocarcinomas correlates with marked inflammatory cell infiltrates and prognosis. J Natl Cancer Inst. 1994;86:120–6.
Espinosa I, Catasus L, D' Angelo E, Mozos A, Pedrola N, Bértolo C, et al. Stromal signatures in endometrioid endometrial carcinomas. Mod Pathol. 2014;27:631–9.
Richardsen E, Uglehus RD, Johnsen SH, Busund LT. Macrophage-colony stimulating factor (CSF1) predicts breast cancer progression and mortality. Anticancer Res. 2015;35:865–74.
Liu H, Zhang H, Shen Z, Lin C, Wang X, Qin J, et al. Increased expression of CSF-1 associates with poor prognosis of patients with gastric cancer undergoing gastrectomy. Medicine. 2016;95:e2675.
Łukaszewicz-Zajac M, Mroczko B, Kozłowski M, Nikliński J, Laudański J, Szmitkowski M. Clinical significance of serum macrophage-colony stimulating factor (M-CSF) in esophageal cancer patients and its comparison with classical tumor markers. Clin Chem Lab Med. 2010;48:1467–73.
Lin H, Lee E, Hestir K, Leo C, Huang M, Bosch E, et al. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science. 2008;320:807–11.
Chihara T, Suzu S, Hassan R, Chutiwitoonchai N, Hiyoshi M, Motoyoshi K, et al. IL-34 and M-CSF share the receptor Fms but are not identical in biological activity and signal activation. Cell Death Differ. 2010;17:1917–27.
Boulakirba S, Pfeifer A, Mhaidly R, Obba S, Goulard M, Schmitt T, et al. IL-34 and CSF-1 display an equivalent macrophage differentiation ability but a different polarization potential. Sci Rep. 2018;8:256.
Rietkötter E, Bleckmann A, Bayerlová M, Menck K, Chuang HN, Wenske B, et al. Anti-CSF-1 treatment is effective to prevent carcinoma invasion induced by monocyte-derived cells but scarcely by microglia. Oncotarget. 2015;6:15482–93.
Ségaliny AI, Mohamadi A, Dizier B, Lokajczyk A, Brion R, Lanel R, et al. Interleukin-34 promotes tumor progression and metastatic process in osteosarcoma through induction of angiogenesis and macrophage recruitment. Int J Cancer. 2015;137:73–85.
Zhou SL, Hu ZQ, Zhou ZJ, Dai Z, Wang Z, Cao Y, et al. miR-28–5p-IL-34-macrophage feedback loop modulates hepatocellular carcinoma metastasis. Hepatology. 2016;63:1560–75.
Franzè E, Dinallo V, Rizzo A, Di Giovangiulio M, Bevivino G, Stolfi C, et al. Interleukin-34 sustains pro-tumorigenic signals in colon cancer tissue. Oncotarget. 2018;9:3432–45.
Baghdadi M, Endo H, Takano A, Ishikawa K, Kameda Y, Wada H, et al. High co-expression of IL-34 and M-CSF correlates with tumor progression and poor survival in lung cancers. Sci Rep. 2018;8:418.
Endo H, Hama N, Baghdadi M, Ishikawa K, Otsuka R, Wada H, et al. Interleukin-34 expression in ovarian cancer: a possible correlation with disease progression. Int Immunol. 2020;32:175–86.
Baghdadi M, Wada H, Nakanishi S, Abe H, Han N, Putra WE, et al. Chemotherapy-induced IL34 enhances immunosuppression by tumor-associated macrophages and mediates survival of chemoresistant lung cancer cells. Cancer Res. 2016;76:6030–42.
Kikuchi T, Mimura K, Okayama H, Nakayama Y, Saito K, Yamada L, et al. A subset of patients with MSS/MSI-low-colorectal cancer showed increased CD8(+) TILs together with up-regulated IFN-γ. Oncol Lett. 2019;18:5977–85.
Endo E, Okayama H, Saito K, Nakajima S, Yamada L, Ujiie D, et al. A TGFβ-dependent stromal subset underlies immune checkpoint inhibitor efficacy in DNA mismatch repair-deficient/microsatellite instability-high colorectal cancer. Mol Cancer Res. 2020;18:1402–13.
Saad RS, Liu YL, Nathan G, Celebrezze J, Medich D, Silverman JF. Endoglin (CD105) and vascular endothelial growth factor as prognostic markers in colorectal cancer. Mod Pathol. 2004;17:197–203.
Hu JM, Liu K, Liu JH, Jiang XL, Wang XL, Yang L, et al. The increased number of tumor-associated macrophage is associated with overexpression of VEGF-C, plays an important role in Kazakh ESCC invasion and metastasis. Exp Mol Pathol. 2017;102:15–21.
Liu J, Li C, Zhang L, Liu K, Jiang X, Wang X, et al. Association of tumour-associated macrophages with cancer cell EMT, invasion, and metastasis of Kazakh oesophageal squamous cell cancer. Diagn Pathol. 2019;14:55.
Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013;6:pl1.
Lelios I, Cansever D, Utz SG, Mildenberger W, Stifter SA, Greter M. Emerging roles of IL-34 in health and disease. J Exp Med. 2020;217:e20190290.
Cioce M, Canino C, Goparaju C, Yang H, Carbone M, Pass HI. Autocrine CSF-1R signaling drives mesothelioma chemoresistance via AKT activation. Cell Death Dis. 2014;5:e1167.
Roos WP, Thomas AD, Kaina B. DNA damage and the balance between survival and death in cancer biology. Nat Rev Cancer. 2016;16:20–33.
Liu A, Yoshioka K, Salerno V, Hsieh P. The mismatch repair-mediated cell cycle checkpoint response to fluorodeoxyuridine. J Cell Biochem. 2008;105:245–54.
Takeuchi M, Tanikawa M, Nagasaka K, Oda K, Kawata Y, Oki S, et al. Anti-tumor effect of inhibition of DNA damage response proteins, ATM and ATR, in endometrial cancer cells. Cancers. 2019;11:1913.
Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 2002;23:549–55.
Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol. 2002;196:254–65.
Shiraishi D, Fujiwara Y, Horlad H, Saito Y, Iriki T, Tsuboki J, et al. CD163 is required for protumoral activation of macrophages in human and murine sarcoma. Cancer Res. 2018;78:3255–66.
Han N, Baghdadi M, Ishikawa K, Endo H, Kobayashi T, Wada H, et al. Enhanced IL-34 expression in nivolumab-resistant metastatic melanoma. Inflamm Regen. 2018;38:3.
Ma X, Lin WY, Chen Y, Stawicki S, Mukhyala K, Wu Y, et al. Structural basis for the dual recognition of helical cytokines IL-34 and CSF-1 by CSF-1R. Structure. 2012;20:676–87.
Foucher ED, Blanchard S, Preisser L, Descamps P, Ifrah N, Delneste Y, et al. IL-34- and M-CSF-induced macrophages switch memory T cells into Th17 cells via membrane IL-1α. Eur J Immunol. 2015;45:1092–102.
Qiao Y, Zhang C, Li A, Wang D, Luo Z, Ping Y, et al. IL6 derived from cancer-associated fibroblasts promotes chemoresistance via CXCR7 in esophageal squamous cell carcinoma. Oncogene. 2018;37:873–83.
Dijkgraaf EM, Heusinkveld M, Tummers B, Vogelpoel LT, Goedemans R, Jha V, et al. Chemotherapy alters monocyte differentiation to favor generation of cancer-supporting M2 macrophages in the tumor microenvironment. Cancer Res. 2013;73:2480–92.
Foucher ED, Blanchard S, Preisser L, Garo E, Ifrah N, Guardiola P, et al. IL-34 induces the differentiation of human monocytes into immunosuppressive macrophages. antagonistic effects of GM-CSF and IFNγ. PLoS One. 2013;8:e56045.
Cassier PA, Italiano A, Gomez-Roca CA, Le Tourneau C, Toulmonde M, Cannarile MA, et al. CSF1R inhibition with emactuzumab in locally advanced diffuse-type tenosynovial giant cell tumours of the soft tissue: a dose-escalation and dose-expansion phase 1 study. Lancet Oncol. 2015;16:949–56.
Hama N, Kobayashi T, Han N, Kitagawa F, Kajihara N, Otsuka R, et al. Interleukin-34 limits the therapeutic effects of immune checkpoint blockade. iScience. 2020;23:101584.
Kudo T, Hamamoto Y, Kato K, Ura T, Kojima T, Tsushima T, et al. Nivolumab treatment for oesophageal squamous-cell carcinoma: an open-label, multicentre, phase 2 trial. Lancet Oncol. 2017;18:631–9.
Takahashi M, Kato K, Okada M, Chin K, Kadowaki S, Hamamoto Y, et al. Nivolumab versus chemotherapy in Japanese patients with advanced esophageal squamous cell carcinoma: a subgroup analysis of a multicenter, randomized, open-label, phase 3 trial (ATTRACTION-3). Esophagus. 2021;18:90–9.

Auteurs

Shotaro Nakajima (S)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.
Department of Medical Electrophysiology, Fukushima Medical University School of Medicine, Fukushima, Japan.

Kosaku Mimura (K)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.
Department of Blood Transfusion and Transplantation Immunology, Fukushima Medical University School of Medicine, Fukushima, Japan.

Katsuharu Saito (K)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Aung Kyi Thar Min (AK)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Eisei Endo (E)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Leo Yamada (L)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Koji Kase (K)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Naoto Yamauchi (N)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Takuro Matsumoto (T)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Hiroshi Nakano (H)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Yasuyuki Kanke (Y)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Hirokazu Okayama (H)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Motonobu Saito (M)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Prajwal Neupane (P)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Zenichiro Saze (Z)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Yohei Watanabe (Y)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Hiroyuki Hanayama (H)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Suguru Hayase (S)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Akinao Kaneta (A)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Tomoyuki Momma (T)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Shinji Ohki (S)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan.

Hiromasa Ohira (H)

Department of Gastroenterology, Fukushima Medical University School of Medicine, Fukushima, Japan.

Koji Kono (K)

Department of Gastrointestinal Tract Surgery, Fukushima Medical University School of Medicine, Fukushima, Japan. kojikono@fmu.ac.jp.

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