Cancer cell-derived interleukin-33 decoy receptor sST2 enhances orthotopic tumor growth in a murine pancreatic cancer model
Proinflammatory interleukin-33 (IL-33) binds to its receptor ST2L and is involved in inflammation and the malignant behavior of cancer cells. However, the role of IL-33-ST2L and the IL-33 decoy receptor sST2 in the tumor microenvironment of pancreatic cancer is unclear. Because we previously reporte...
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Published in | PloS one Vol. 15; no. 4; p. e0232230 |
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27.04.2020
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Abstract | Proinflammatory interleukin-33 (IL-33) binds to its receptor ST2L and is involved in inflammation and the malignant behavior of cancer cells. However, the role of IL-33-ST2L and the IL-33 decoy receptor sST2 in the tumor microenvironment of pancreatic cancer is unclear. Because we previously reported that sST2 derived from colon cancer cells profoundly influences malignant tumor growth, we hypothesized that sST2 released from pancreatic cancer cells also modulates IL-33-ST2L signaling in the tumor microenvironment, thereby influencing tumor growth.
ST2 (ST2L and sST2) expression in mouse pancreatic cancer Panc02 cells was downregulated by shRNAs. mRNA expression levels of IL-33, ST2, cytokines and chemokines in the cells and tumor tissues were examined using real-time PCR. sST2 secretion and the amount of CXCL3 in tumor tissues were measured using ELISA. Tumor growth was investigated after injection of the cells into the pancreas of C57BL/6 mice. MPO+, F4/80+ and CD20+ cells in tumor tissues were detected using immunohistochemistry.
Some but not all human and mouse pancreatic cancer cell lines preferentially expressed sST2. Then, we investigated the role of sST2 in orthotopic tumor growth of sST2-expressing mouse pancreatic cancer Panc02 cells in immunocompetent mice. shRNA-mediated knockdown of sST2 expression in the cells suppressed orthotopic tumor growth, which was partially recovered by overexpression of shRNA-resistant sST2 mRNA but was not evident in IL-33 knockout mice. This was associated with decreases in Cxcl3 expression, vessel density and accumulation of cancer-associated neutrophils but not cancer-associated macrophages. Administration of SB225002, an inhibitor of the CXCL3 receptor CXCR2, induced similar effects.
Cancer cell-derived sST2 enhances tumor growth through upregulation of CXCL3 via inhibition of IL-33-ST2L signaling in the tumor microenvironment of pancreatic cancer. These results suggest that the sST2 and the CXCL3-CXCR2 axis could be therapeutic targets. |
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AbstractList | Proinflammatory interleukin-33 (IL-33) binds to its receptor ST2L and is involved in inflammation and the malignant behavior of cancer cells. However, the role of IL-33-ST2L and the IL-33 decoy receptor sST2 in the tumor microenvironment of pancreatic cancer is unclear. Because we previously reported that sST2 derived from colon cancer cells profoundly influences malignant tumor growth, we hypothesized that sST2 released from pancreatic cancer cells also modulates IL-33-ST2L signaling in the tumor microenvironment, thereby influencing tumor growth.
ST2 (ST2L and sST2) expression in mouse pancreatic cancer Panc02 cells was downregulated by shRNAs. mRNA expression levels of IL-33, ST2, cytokines and chemokines in the cells and tumor tissues were examined using real-time PCR. sST2 secretion and the amount of CXCL3 in tumor tissues were measured using ELISA. Tumor growth was investigated after injection of the cells into the pancreas of C57BL/6 mice. MPO+, F4/80+ and CD20+ cells in tumor tissues were detected using immunohistochemistry.
Some but not all human and mouse pancreatic cancer cell lines preferentially expressed sST2. Then, we investigated the role of sST2 in orthotopic tumor growth of sST2-expressing mouse pancreatic cancer Panc02 cells in immunocompetent mice. shRNA-mediated knockdown of sST2 expression in the cells suppressed orthotopic tumor growth, which was partially recovered by overexpression of shRNA-resistant sST2 mRNA but was not evident in IL-33 knockout mice. This was associated with decreases in Cxcl3 expression, vessel density and accumulation of cancer-associated neutrophils but not cancer-associated macrophages. Administration of SB225002, an inhibitor of the CXCL3 receptor CXCR2, induced similar effects.
Cancer cell-derived sST2 enhances tumor growth through upregulation of CXCL3 via inhibition of IL-33-ST2L signaling in the tumor microenvironment of pancreatic cancer. These results suggest that the sST2 and the CXCL3-CXCR2 axis could be therapeutic targets. Proinflammatory interleukin-33 (IL-33) binds to its receptor ST2L and is involved in inflammation and the malignant behavior of cancer cells. However, the role of IL-33-ST2L and the IL-33 decoy receptor sST2 in the tumor microenvironment of pancreatic cancer is unclear. Because we previously reported that sST2 derived from colon cancer cells profoundly influences malignant tumor growth, we hypothesized that sST2 released from pancreatic cancer cells also modulates IL-33-ST2L signaling in the tumor microenvironment, thereby influencing tumor growth. ST2 (ST2L and sST2) expression in mouse pancreatic cancer Panc02 cells was downregulated by shRNAs. mRNA expression levels of IL-33, ST2, cytokines and chemokines in the cells and tumor tissues were examined using real-time PCR. sST2 secretion and the amount of CXCL3 in tumor tissues were measured using ELISA. Tumor growth was investigated after injection of the cells into the pancreas of C57BL/6 mice. MPO.sup.+, F4/80.sup.+ and CD20.sup.+ cells in tumor tissues were detected using immunohistochemistry. Some but not all human and mouse pancreatic cancer cell lines preferentially expressed sST2. Then, we investigated the role of sST2 in orthotopic tumor growth of sST2-expressing mouse pancreatic cancer Panc02 cells in immunocompetent mice. shRNA-mediated knockdown of sST2 expression in the cells suppressed orthotopic tumor growth, which was partially recovered by overexpression of shRNA-resistant sST2 mRNA but was not evident in IL-33 knockout mice. This was associated with decreases in Cxcl3 expression, vessel density and accumulation of cancer-associated neutrophils but not cancer-associated macrophages. Administration of SB225002, an inhibitor of the CXCL3 receptor CXCR2, induced similar effects. Cancer cell-derived sST2 enhances tumor growth through upregulation of CXCL3 via inhibition of IL-33-ST2L signaling in the tumor microenvironment of pancreatic cancer. These results suggest that the sST2 and the CXCL3-CXCR2 axis could be therapeutic targets. Background Proinflammatory interleukin-33 (IL-33) binds to its receptor ST2L and is involved in inflammation and the malignant behavior of cancer cells. However, the role of IL-33-ST2L and the IL-33 decoy receptor sST2 in the tumor microenvironment of pancreatic cancer is unclear. Because we previously reported that sST2 derived from colon cancer cells profoundly influences malignant tumor growth, we hypothesized that sST2 released from pancreatic cancer cells also modulates IL-33-ST2L signaling in the tumor microenvironment, thereby influencing tumor growth. Methods ST2 (ST2L and sST2) expression in mouse pancreatic cancer Panc02 cells was downregulated by shRNAs. mRNA expression levels of IL-33, ST2, cytokines and chemokines in the cells and tumor tissues were examined using real-time PCR. sST2 secretion and the amount of CXCL3 in tumor tissues were measured using ELISA. Tumor growth was investigated after injection of the cells into the pancreas of C57BL/6 mice. MPO.sup.+, F4/80.sup.+ and CD20.sup.+ cells in tumor tissues were detected using immunohistochemistry. Results Some but not all human and mouse pancreatic cancer cell lines preferentially expressed sST2. Then, we investigated the role of sST2 in orthotopic tumor growth of sST2-expressing mouse pancreatic cancer Panc02 cells in immunocompetent mice. shRNA-mediated knockdown of sST2 expression in the cells suppressed orthotopic tumor growth, which was partially recovered by overexpression of shRNA-resistant sST2 mRNA but was not evident in IL-33 knockout mice. This was associated with decreases in Cxcl3 expression, vessel density and accumulation of cancer-associated neutrophils but not cancer-associated macrophages. Administration of SB225002, an inhibitor of the CXCL3 receptor CXCR2, induced similar effects. Conclusions Cancer cell-derived sST2 enhances tumor growth through upregulation of CXCL3 via inhibition of IL-33-ST2L signaling in the tumor microenvironment of pancreatic cancer. These results suggest that the sST2 and the CXCL3-CXCR2 axis could be therapeutic targets. Background Proinflammatory interleukin-33 (IL-33) binds to its receptor ST2L and is involved in inflammation and the malignant behavior of cancer cells. However, the role of IL-33-ST2L and the IL-33 decoy receptor sST2 in the tumor microenvironment of pancreatic cancer is unclear. Because we previously reported that sST2 derived from colon cancer cells profoundly influences malignant tumor growth, we hypothesized that sST2 released from pancreatic cancer cells also modulates IL-33-ST2L signaling in the tumor microenvironment, thereby influencing tumor growth. Methods ST2 (ST2L and sST2) expression in mouse pancreatic cancer Panc02 cells was downregulated by shRNAs. mRNA expression levels of IL-33, ST2, cytokines and chemokines in the cells and tumor tissues were examined using real-time PCR. sST2 secretion and the amount of CXCL3 in tumor tissues were measured using ELISA. Tumor growth was investigated after injection of the cells into the pancreas of C57BL/6 mice. MPO+, F4/80+ and CD20+ cells in tumor tissues were detected using immunohistochemistry. Results Some but not all human and mouse pancreatic cancer cell lines preferentially expressed sST2. Then, we investigated the role of sST2 in orthotopic tumor growth of sST2-expressing mouse pancreatic cancer Panc02 cells in immunocompetent mice. shRNA-mediated knockdown of sST2 expression in the cells suppressed orthotopic tumor growth, which was partially recovered by overexpression of shRNA-resistant sST2 mRNA but was not evident in IL-33 knockout mice. This was associated with decreases in Cxcl3 expression, vessel density and accumulation of cancer-associated neutrophils but not cancer-associated macrophages. Administration of SB225002, an inhibitor of the CXCL3 receptor CXCR2, induced similar effects. Conclusions Cancer cell-derived sST2 enhances tumor growth through upregulation of CXCL3 via inhibition of IL-33-ST2L signaling in the tumor microenvironment of pancreatic cancer. These results suggest that the sST2 and the CXCL3-CXCR2 axis could be therapeutic targets. BackgroundProinflammatory interleukin-33 (IL-33) binds to its receptor ST2L and is involved in inflammation and the malignant behavior of cancer cells. However, the role of IL-33-ST2L and the IL-33 decoy receptor sST2 in the tumor microenvironment of pancreatic cancer is unclear. Because we previously reported that sST2 derived from colon cancer cells profoundly influences malignant tumor growth, we hypothesized that sST2 released from pancreatic cancer cells also modulates IL-33-ST2L signaling in the tumor microenvironment, thereby influencing tumor growth.MethodsST2 (ST2L and sST2) expression in mouse pancreatic cancer Panc02 cells was downregulated by shRNAs. mRNA expression levels of IL-33, ST2, cytokines and chemokines in the cells and tumor tissues were examined using real-time PCR. sST2 secretion and the amount of CXCL3 in tumor tissues were measured using ELISA. Tumor growth was investigated after injection of the cells into the pancreas of C57BL/6 mice. MPO+, F4/80+ and CD20+ cells in tumor tissues were detected using immunohistochemistry.ResultsSome but not all human and mouse pancreatic cancer cell lines preferentially expressed sST2. Then, we investigated the role of sST2 in orthotopic tumor growth of sST2-expressing mouse pancreatic cancer Panc02 cells in immunocompetent mice. shRNA-mediated knockdown of sST2 expression in the cells suppressed orthotopic tumor growth, which was partially recovered by overexpression of shRNA-resistant sST2 mRNA but was not evident in IL-33 knockout mice. This was associated with decreases in Cxcl3 expression, vessel density and accumulation of cancer-associated neutrophils but not cancer-associated macrophages. Administration of SB225002, an inhibitor of the CXCL3 receptor CXCR2, induced similar effects.ConclusionsCancer cell-derived sST2 enhances tumor growth through upregulation of CXCL3 via inhibition of IL-33-ST2L signaling in the tumor microenvironment of pancreatic cancer. These results suggest that the sST2 and the CXCL3-CXCR2 axis could be therapeutic targets. Background Proinflammatory interleukin-33 (IL-33) binds to its receptor ST2L and is involved in inflammation and the malignant behavior of cancer cells. However, the role of IL-33-ST2L and the IL-33 decoy receptor sST2 in the tumor microenvironment of pancreatic cancer is unclear. Because we previously reported that sST2 derived from colon cancer cells profoundly influences malignant tumor growth, we hypothesized that sST2 released from pancreatic cancer cells also modulates IL-33-ST2L signaling in the tumor microenvironment, thereby influencing tumor growth. Methods ST2 (ST2L and sST2) expression in mouse pancreatic cancer Panc02 cells was downregulated by shRNAs. mRNA expression levels of IL-33, ST2, cytokines and chemokines in the cells and tumor tissues were examined using real-time PCR. sST2 secretion and the amount of CXCL3 in tumor tissues were measured using ELISA. Tumor growth was investigated after injection of the cells into the pancreas of C57BL/6 mice. MPO+, F4/80+ and CD20+ cells in tumor tissues were detected using immunohistochemistry. Results Some but not all human and mouse pancreatic cancer cell lines preferentially expressed sST2. Then, we investigated the role of sST2 in orthotopic tumor growth of sST2-expressing mouse pancreatic cancer Panc02 cells in immunocompetent mice. shRNA-mediated knockdown of sST2 expression in the cells suppressed orthotopic tumor growth, which was partially recovered by overexpression of shRNA-resistant sST2 mRNA but was not evident in IL-33 knockout mice. This was associated with decreases in Cxcl3 expression, vessel density and accumulation of cancer-associated neutrophils but not cancer-associated macrophages. Administration of SB225002, an inhibitor of the CXCL3 receptor CXCR2, induced similar effects. Conclusions Cancer cell-derived sST2 enhances tumor growth through upregulation of CXCL3 via inhibition of IL-33-ST2L signaling in the tumor microenvironment of pancreatic cancer. These results suggest that the sST2 and the CXCL3-CXCR2 axis could be therapeutic targets. |
Audience | Academic |
Author | Koshikawa, Nobuko Nagase, Hiroki Takenaga, Keizo Akimoto, Miho |
AuthorAffiliation | University of Miami, UNITED STATES 1 Laboratory of Cancer Genetics, Chiba Cancer Center Research Institute, Nitona, Chuoh-ku, Chiba, Japan 2 Department of Biochemistry, Teikyo University School of Medicine, Kaga, Itabashi-ku, Tokyo, Japan |
AuthorAffiliation_xml | – name: University of Miami, UNITED STATES – name: 2 Department of Biochemistry, Teikyo University School of Medicine, Kaga, Itabashi-ku, Tokyo, Japan – name: 1 Laboratory of Cancer Genetics, Chiba Cancer Center Research Institute, Nitona, Chuoh-ku, Chiba, Japan |
Author_xml | – sequence: 1 givenname: Keizo orcidid: 0000-0001-9127-2965 surname: Takenaga fullname: Takenaga, Keizo organization: Laboratory of Cancer Genetics, Chiba Cancer Center Research Institute, Nitona, Chuoh-ku, Chiba, Japan – sequence: 2 givenname: Miho surname: Akimoto fullname: Akimoto, Miho organization: Department of Biochemistry, Teikyo University School of Medicine, Kaga, Itabashi-ku, Tokyo, Japan – sequence: 3 givenname: Nobuko surname: Koshikawa fullname: Koshikawa, Nobuko organization: Laboratory of Cancer Genetics, Chiba Cancer Center Research Institute, Nitona, Chuoh-ku, Chiba, Japan – sequence: 4 givenname: Hiroki surname: Nagase fullname: Nagase, Hiroki organization: Laboratory of Cancer Genetics, Chiba Cancer Center Research Institute, Nitona, Chuoh-ku, Chiba, Japan |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32340025$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1371_journal_pone_0270677 crossref_primary_10_1073_pnas_2218033120 crossref_primary_10_1007_s12032_021_01590_y crossref_primary_10_1016_j_cyto_2022_155961 crossref_primary_10_3390_cancers12123787 crossref_primary_10_1016_j_lfs_2024_122691 crossref_primary_10_1177_15353702221102094 crossref_primary_10_3390_cells10061385 crossref_primary_10_17352_oja_000015 |
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Snippet | Proinflammatory interleukin-33 (IL-33) binds to its receptor ST2L and is involved in inflammation and the malignant behavior of cancer cells. However, the role... Background Proinflammatory interleukin-33 (IL-33) binds to its receptor ST2L and is involved in inflammation and the malignant behavior of cancer cells.... BACKGROUNDProinflammatory interleukin-33 (IL-33) binds to its receptor ST2L and is involved in inflammation and the malignant behavior of cancer cells.... BackgroundProinflammatory interleukin-33 (IL-33) binds to its receptor ST2L and is involved in inflammation and the malignant behavior of cancer cells.... Background Proinflammatory interleukin-33 (IL-33) binds to its receptor ST2L and is involved in inflammation and the malignant behavior of cancer cells.... |
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SubjectTerms | Biology and Life Sciences Cancer cells CD20 antigen Chemokines Colon Colon cancer Colorectal cancer CXCR2 protein Cytokines Enzyme-linked immunosorbent assay Fibroblasts Gene expression Growth House mouse Immunohistochemistry Inflammation Interleukins Laboratory animals Leukocytes (neutrophilic) Macrophages Medicine and Health Sciences Messenger RNA Pancreas Pancreatic cancer Pharmaceutical industry R&D Receptors Research & development Research and Analysis Methods RNA Signaling Therapeutic applications Time Tissues Tumor cell lines Tumors |
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Title | Cancer cell-derived interleukin-33 decoy receptor sST2 enhances orthotopic tumor growth in a murine pancreatic cancer model |
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