Molecular Profiling Reveals a Tumor-Promoting Phenotype of Monocytes and Macrophages in Human Cancer Progression
Monocytes and macrophages are major components of the tumor microenvironment, but their contributions to human cancer are poorly understood. We used molecular profiling combined with functional assays to investigate the role of these cells in human renal cell carcinoma (RCC). Blood monocytes from RC...
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Published in | Immunity (Cambridge, Mass.) Vol. 41; no. 5; pp. 815 - 829 |
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Main Authors | , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Elsevier Inc
20.11.2014
Elsevier Limited |
Subjects | |
Online Access | Get full text |
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Abstract | Monocytes and macrophages are major components of the tumor microenvironment, but their contributions to human cancer are poorly understood. We used molecular profiling combined with functional assays to investigate the role of these cells in human renal cell carcinoma (RCC). Blood monocytes from RCC patients displayed a tumor-promoting transcriptional profile that supported functions like angiogenesis and invasion. Induction of this protumor phenotype required an interleukin-1 receptor (IL-1R)-dependent mechanism. Indeed, targeting of IL-1-IL-1R axis in a human RCC xenograft model abrogated the protumor phenotype of tumor-associated macrophages (TAMs) and reduced tumor growth in vivo. Supporting this, meta-analysis of gene expression from human RCC tumors showed IL1B expression to correlate with myelomonocytic markers, protumor genes, and tumor staging. Analyzing RCC patient tumors confirmed the protumor phenotype of TAMs. These data provide direct evidence for a tumor-promoting role of monocytes and macrophages in human cancer and indicate IL-1-IL-1R as a possible therapeutic target.
•Monocytes and macrophages show a protumor phenotype in a human cancer setting•The protumor phenotype is regulated by an IL-1 receptor-dependent mechanism•Targeting this mechanism abrogated macrophage protumor phenotype and tumor in vivo
Monocytes and macrophages are major components of the tumor microenvironment, but their contributions to human cancer are poorly understood. Biswas and colleagues provide transcriptional, functional, and mechanistic data demonstrating a tumor-promoting phenotype of these cells in a human cancer setting. |
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AbstractList | Monocytes and macrophages are major components of the tumor microenvironment, but their contributions to human cancer are poorly understood. We used molecular profiling combined with functional assays to investigate the role of these cells in human renal cell carcinoma (RCC). Blood monocytes from RCC patients displayed a tumor-promoting transcriptional profile that supported functions like angiogenesis and invasion. Induction of this protumor phenotype required an interleukin-1 receptor (IL-1R)-dependent mechanism. Indeed, targeting of IL-1-IL-1R axis in a human RCC xenograft model abrogated the protumor phenotype of tumor-associated macrophages (TAMs) and reduced tumor growth in vivo. Supporting this, meta-analysis of gene expression from human RCC tumors showed IL1B expression to correlate with myelomonocytic markers, protumor genes, and tumor staging. Analyzing RCC patient tumors confirmed the protumor phenotype of TAMs. These data provide direct evidence for a tumor-promoting role of monocytes and macrophages in human cancer and indicate IL-1-IL-1R as a possible therapeutic target. Monocytes and macrophages are major components of the tumor microenvironment, but their contributions to human cancer are poorly understood. We used molecular profiling combined with functional assays to investigate the role of these cells in human renal cell carcinoma (RCC). Blood monocytes from RCC patients displayed a tumor-promoting transcriptional profile that supported functions like angiogenesis and invasion. Induction of this protumor phenotype required an interleukin-1 receptor (IL-1R)-dependent mechanism. Indeed, targeting of IL-1-IL-1R axis in a human RCC xenograft model abrogated the protumor phenotype of tumor-associated macrophages (TAMs) and reduced tumor growth in vivo. Supporting this, meta-analysis of gene expression from human RCC tumors showedIL1Bexpression to correlate with myelomonocytic markers, protumor genes, and tumor staging. Analyzing RCC patient tumors confirmed the protumor phenotype of TAMs. These data provide direct evidence for a tumor-promoting role of monocytes and macrophages in human cancer and indicate IL-1-IL-1R as a possible therapeutic target. Monocytes and macrophages are major components of the tumor microenvironment, but their contributions to human cancer are poorly understood. We used molecular profiling combined with functional assays to investigate the role of these cells in human renal cell carcinoma (RCC). Blood monocytes from RCC patients displayed a tumor-promoting transcriptional profile that supported functions like angiogenesis and invasion. Induction of this protumor phenotype required an interleukin-1 receptor (IL-1R)-dependent mechanism. Indeed, targeting of IL-1-IL-1R axis in a human RCC xenograft model abrogated the protumor phenotype of tumor-associated macrophages (TAMs) and reduced tumor growth in vivo. Supporting this, meta-analysis of gene expression from human RCC tumors showed IL1B expression to correlate with myelomonocytic markers, protumor genes, and tumor staging. Analyzing RCC patient tumors confirmed the protumor phenotype of TAMs. These data provide direct evidence for a tumor-promoting role of monocytes and macrophages in human cancer and indicate IL-1-IL-1R as a possible therapeutic target. •Monocytes and macrophages show a protumor phenotype in a human cancer setting•The protumor phenotype is regulated by an IL-1 receptor-dependent mechanism•Targeting this mechanism abrogated macrophage protumor phenotype and tumor in vivo Monocytes and macrophages are major components of the tumor microenvironment, but their contributions to human cancer are poorly understood. Biswas and colleagues provide transcriptional, functional, and mechanistic data demonstrating a tumor-promoting phenotype of these cells in a human cancer setting. Monocytes and macrophages are major components of the tumor microenvironment, but their contributions to human cancer are poorly understood. We used molecular profiling combined with functional assays to investigate the role of these cells in human renal cell carcinoma (RCC). Blood monocytes from RCC patients displayed a tumor-promoting transcriptional profile that supported functions like angiogenesis and invasion. Induction of this protumor phenotype required an interleukin-1 receptor (IL-1R)-dependent mechanism. Indeed, targeting of IL-1-IL-1R axis in a human RCC xenograft model abrogated the protumor phenotype of tumor-associated macrophages (TAMs) and reduced tumor growth in vivo. Supporting this, meta-analysis of gene expression from human RCC tumors showed IL1B expression to correlate with myelomonocytic markers, protumor genes, and tumor staging. Analyzing RCC patient tumors confirmed the protumor phenotype of TAMs. These data provide direct evidence for a tumor-promoting role of monocytes and macrophages in human cancer and indicate IL-1-IL-1R as a possible therapeutic target. |
Author | Thamboo, Thomas Paulraj Chiong, Edmund Dhillon, Manprit Kaur Yang, Henry Van Ginderachter, Jo A. Shalova, Irina N. Laoui, Damya Kamaraj, Revathy Teo, Yi Ling Lim, Jyue Yuan Poidinger, Michael Chittezhath, Manesh Chen, Jinmiao Raman, Lata Biswas, Subhra K. Wong, Alvin S.C. Lum, Josephine Zolezzi, Francesca |
Author_xml | – sequence: 1 givenname: Manesh surname: Chittezhath fullname: Chittezhath, Manesh organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Biopolis, Singapore 138648, Singapore – sequence: 2 givenname: Manprit Kaur surname: Dhillon fullname: Dhillon, Manprit Kaur organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Biopolis, Singapore 138648, Singapore – sequence: 3 givenname: Jyue Yuan surname: Lim fullname: Lim, Jyue Yuan organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Biopolis, Singapore 138648, Singapore – sequence: 4 givenname: Damya surname: Laoui fullname: Laoui, Damya organization: Laboratory of Myeloid Cell Immunology, VIB, Brussels 1050, Belgium – sequence: 5 givenname: Irina N. surname: Shalova fullname: Shalova, Irina N. organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Biopolis, Singapore 138648, Singapore – sequence: 6 givenname: Yi Ling surname: Teo fullname: Teo, Yi Ling organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Biopolis, Singapore 138648, Singapore – sequence: 7 givenname: Jinmiao surname: Chen fullname: Chen, Jinmiao organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Biopolis, Singapore 138648, Singapore – sequence: 8 givenname: Revathy surname: Kamaraj fullname: Kamaraj, Revathy organization: Department of Urology, National University Health System, Lower Kent Ridge Road, Singapore 119074, Singapore – sequence: 9 givenname: Lata surname: Raman fullname: Raman, Lata organization: Department of Urology, National University Health System, Lower Kent Ridge Road, Singapore 119074, Singapore – sequence: 10 givenname: Josephine surname: Lum fullname: Lum, Josephine organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Biopolis, Singapore 138648, Singapore – sequence: 11 givenname: Thomas Paulraj surname: Thamboo fullname: Thamboo, Thomas Paulraj organization: Department of Pathology, National University Health System, Lower Kent Ridge Road, Singapore 119074, Singapore – sequence: 12 givenname: Edmund surname: Chiong fullname: Chiong, Edmund organization: Department of Urology, National University Health System, Lower Kent Ridge Road, Singapore 119074, Singapore – sequence: 13 givenname: Francesca surname: Zolezzi fullname: Zolezzi, Francesca organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Biopolis, Singapore 138648, Singapore – sequence: 14 givenname: Henry surname: Yang fullname: Yang, Henry organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Biopolis, Singapore 138648, Singapore – sequence: 15 givenname: Jo A. surname: Van Ginderachter fullname: Van Ginderachter, Jo A. organization: Laboratory of Myeloid Cell Immunology, VIB, Brussels 1050, Belgium – sequence: 16 givenname: Michael surname: Poidinger fullname: Poidinger, Michael organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Biopolis, Singapore 138648, Singapore – sequence: 17 givenname: Alvin S.C. surname: Wong fullname: Wong, Alvin S.C. organization: Department of Haematology-Oncology, National University Health System, Lower Kent Ridge Road, Singapore 119074, Singapore – sequence: 18 givenname: Subhra K. surname: Biswas fullname: Biswas, Subhra K. email: subhra_biswas@immunol.a-star.edu.sg organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Biopolis, Singapore 138648, Singapore |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25453823$$D View this record in MEDLINE/PubMed |
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Copyright | 2014 Elsevier Inc. Copyright © 2014 Elsevier Inc. All rights reserved. Copyright Elsevier Limited Nov 20, 2014 |
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SubjectTerms | Animals Cancer Cancer therapies Carcinoma, Renal Cell - immunology Cell Proliferation - genetics Chemokines Cytokines - biosynthesis Cytokines - immunology Gene expression Gene Expression Profiling Genotype & phenotype Humans Inflammation - immunology Interleukin 1 Receptor Antagonist Protein - pharmacology Interleukin-1beta - antagonists & inhibitors Interleukin-1beta - biosynthesis Interleukin-1beta - genetics Interleukin-1beta - immunology Kinases Ligands Macrophages - immunology Medical prognosis Medical research Metastasis Mice Mice, Knockout Mice, SCID Monocytes - immunology Myeloid Differentiation Factor 88 Neoplasm Transplantation Neovascularization, Pathologic Principal components analysis Receptors, Interleukin-1 - antagonists & inhibitors Receptors, Interleukin-1 - genetics Receptors, Interleukin-1 - immunology Transcription Factor RelA - genetics Transplantation, Heterologous Tumor Cells, Cultured |
Title | Molecular Profiling Reveals a Tumor-Promoting Phenotype of Monocytes and Macrophages in Human Cancer Progression |
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