Multimodal imaging of the tumor microenvironment and biological responses to immune therapy
Beyond heterogeneous cancer cells, the tumor microenvironment includes stromal and immune cells, blood vessels, extracellular matrix and biologically active molecules. Abnormal signaling, uncontrolled proliferation and high interstitial pressure all contribute to a chaotic, non-hierarchical vascular...
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Published in | Biomedical microdevices Vol. 20; no. 4; p. 105 |
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Main Authors | , , , |
Format | Journal Article |
Language | English |
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Springer US
03.12.2018
Springer Nature B.V |
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Abstract | Beyond heterogeneous cancer cells, the tumor microenvironment includes stromal and immune cells, blood vessels, extracellular matrix and biologically active molecules. Abnormal signaling, uncontrolled proliferation and high interstitial pressure all contribute to a chaotic, non-hierarchical vascular organization. Using an immune competent 4T1 breast adenocarcinoma murine model, this study fully characterizes the architecture and immunocyte milieu of the tumor microenvironment. Heterogeneous vessel distribution, chaotic connectivity, limited perfusion, cancer cell density, immune phenotype, and biological responses to immune therapy are presented. Cancer cell density mirrored the distribution of large, perfusable vessels, both predominately in the tumor periphery. Intratumoral administration of the proinflammatory cytokine IL-12 led to an increase in CD45
+
leukocytes, with a specific increase in CD4
+
and CD8
+
T cells, and a decrease in the percentage of Gr-l
lo
myeloid-derived suppressor cells. Concomitantly, serum G-CSF, IL-10 and VEGF decreased, while CXCR9 and interferon gamma increased. The distribution pattern of infiltrating monocytes/macrophages, visualized using a fluorescent perfluorocarbon emulsion, indicated that macrophages predominately localize in the vicinity of large blood vessels. Electron microscopy supports the presence of dense tumor cell masses throughout the tumor, with the largest vessels present in the surrounding mammary fat pad. Overall, large vessels in the 4T1 tumor periphery support high, localized vascular perfusion and myeloid accumulation. The pro-inflammatory cytokine IL-12 stimulated a transition towards T helper 1 cytokines in serum, supporting suppression of tumor growth and angiostatic conditions. |
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AbstractList | Beyond heterogeneous cancer cells, the tumor microenvironment includes stromal and immune cells, blood vessels, extracellular matrix and biologically active molecules. Abnormal signaling, uncontrolled proliferation and high interstitial pressure all contribute to a chaotic, non-hierarchical vascular organization. Using an immune competent 4T1 breast adenocarcinoma murine model, this study fully characterizes the architecture and immunocyte milieu of the tumor microenvironment. Heterogeneous vessel distribution, chaotic connectivity, limited perfusion, cancer cell density, immune phenotype, and biological responses to immune therapy are presented. Cancer cell density mirrored the distribution of large, perfusable vessels, both predominately in the tumor periphery. Intratumoral administration of the proinflammatory cytokine IL-12 led to an increase in CD45
+
leukocytes, with a specific increase in CD4
+
and CD8
+
T cells, and a decrease in the percentage of Gr-l
lo
myeloid-derived suppressor cells. Concomitantly, serum G-CSF and VEGF decreased, while CXCR9 and interferon gamma increased. The distribution pattern of infiltrating monocytes/macrophages, visualized using a fluorescent perfluorocarbon emulsion, indicated that macrophages predominately localize in the vicinity of large blood vessels. Electron microscopy supports the presence of dense tumor cell masses throughout the tumor, with the largest vessels present in the surrounding mammary fat pad. Overall, the large vessels in the 4T1 tumor periphery support high vascular perfusion and myeloid accumulation. The pro-inflammatory cytokine IL-12 stimulated a transition towards T helper 1 cytokines within the tumor and in serum, supporting suppression of tumor growth and angiostatic conditions. Beyond heterogeneous cancer cells, the tumor microenvironment includes stromal and immune cells, blood vessels, extracellular matrix and biologically active molecules. Abnormal signaling, uncontrolled proliferation and high interstitial pressure all contribute to a chaotic, non-hierarchical vascular organization. Using an immune competent 4T1 breast adenocarcinoma murine model, this study fully characterizes the architecture and immunocyte milieu of the tumor microenvironment. Heterogeneous vessel distribution, chaotic connectivity, limited perfusion, cancer cell density, immune phenotype, and biological responses to immune therapy are presented. Cancer cell density mirrored the distribution of large, perfusable vessels, both predominately in the tumor periphery. Intratumoral administration of the proinflammatory cytokine IL-12 led to an increase in CD45 + leukocytes, with a specific increase in CD4 + and CD8 + T cells, and a decrease in the percentage of Gr-l lo myeloid-derived suppressor cells. Concomitantly, serum G-CSF, IL-10 and VEGF decreased, while CXCR9 and interferon gamma increased. The distribution pattern of infiltrating monocytes/macrophages, visualized using a fluorescent perfluorocarbon emulsion, indicated that macrophages predominately localize in the vicinity of large blood vessels. Electron microscopy supports the presence of dense tumor cell masses throughout the tumor, with the largest vessels present in the surrounding mammary fat pad. Overall, large vessels in the 4T1 tumor periphery support high, localized vascular perfusion and myeloid accumulation. The pro-inflammatory cytokine IL-12 stimulated a transition towards T helper 1 cytokines in serum, supporting suppression of tumor growth and angiostatic conditions. Beyond heterogeneous cancer cells, the tumor microenvironment includes stromal and immune cells, blood vessels, extracellular matrix and biologically active molecules. Abnormal signaling, uncontrolled proliferation and high interstitial pressure all contribute to a chaotic, non-hierarchical vascular organization. Using an immune competent 4T1 breast adenocarcinoma murine model, this study fully characterizes the architecture and immunocyte milieu of the tumor microenvironment. Heterogeneous vessel distribution, chaotic connectivity, limited perfusion, cancer cell density, immune phenotype, and biological responses to immune therapy are presented. Cancer cell density mirrored the distribution of large, perfusable vessels, both predominately in the tumor periphery. Intratumoral administration of the proinflammatory cytokine IL-12 led to an increase in CD45+ leukocytes, with a specific increase in CD4+ and CD8+ T cells, and a decrease in the percentage of Gr-llo myeloid-derived suppressor cells. Concomitantly, serum G-CSF, IL-10 and VEGF decreased, while CXCR9 and interferon gamma increased. The distribution pattern of infiltrating monocytes/macrophages, visualized using a fluorescent perfluorocarbon emulsion, indicated that macrophages predominately localize in the vicinity of large blood vessels. Electron microscopy supports the presence of dense tumor cell masses throughout the tumor, with the largest vessels present in the surrounding mammary fat pad. Overall, large vessels in the 4T1 tumor periphery support high, localized vascular perfusion and myeloid accumulation. The pro-inflammatory cytokine IL-12 stimulated a transition towards T helper 1 cytokines in serum, supporting suppression of tumor growth and angiostatic conditions. Beyond heterogeneous cancer cells, the tumor microenvironment includes stromal and immune cells, blood vessels, extracellular matrix and biologically active molecules. Abnormal signaling, uncontrolled proliferation and high interstitial pressure all contribute to a chaotic, non-hierarchical vascular organization. Using an immune competent 4T1 breast adenocarcinoma murine model, this study fully characterizes the architecture and immunocyte milieu of the tumor microenvironment. Heterogeneous vessel distribution, chaotic connectivity, limited perfusion, cancer cell density, immune phenotype, and biological responses to immune therapy are presented. Cancer cell density mirrored the distribution of large, perfusable vessels, both predominately in the tumor periphery. Intratumoral administration of the proinflammatory cytokine IL-12 led to an increase in CD45 leukocytes, with a specific increase in CD4 and CD8 T cells, and a decrease in the percentage of Gr-l myeloid-derived suppressor cells. Concomitantly, serum G-CSF, IL-10 and VEGF decreased, while CXCR9 and interferon gamma increased. The distribution pattern of infiltrating monocytes/macrophages, visualized using a fluorescent perfluorocarbon emulsion, indicated that macrophages predominately localize in the vicinity of large blood vessels. Electron microscopy supports the presence of dense tumor cell masses throughout the tumor, with the largest vessels present in the surrounding mammary fat pad. Overall, large vessels in the 4T1 tumor periphery support high, localized vascular perfusion and myeloid accumulation. The pro-inflammatory cytokine IL-12 stimulated a transition towards T helper 1 cytokines in serum, supporting suppression of tumor growth and angiostatic conditions. |
ArticleNumber | 105 |
Author | De La Cerda, Jorge Saucedo, Alexander M. Suami, Hiroo Serda, Rita E. |
AuthorAffiliation | 3 UT D Anderson Cancer Center, Department of Plastic Surgery, Houston, TX 77030, USA 4 Medicine and Health Sciences, Macquarie University, Sydney NSW, Australia 1 Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston, TX 77030, USA 6 Internal Medicine, University of New Mexico, Albuquerque, NM 87131, USA 5 Department of Nanomedicine, Houston Methodist, Houston, TX 77030, USA 2 UT D Anderson Cancer Center, Small Animal Imaging Resource, Houston, TX 77030, USA |
AuthorAffiliation_xml | – name: 2 UT D Anderson Cancer Center, Small Animal Imaging Resource, Houston, TX 77030, USA – name: 6 Internal Medicine, University of New Mexico, Albuquerque, NM 87131, USA – name: 5 Department of Nanomedicine, Houston Methodist, Houston, TX 77030, USA – name: 4 Medicine and Health Sciences, Macquarie University, Sydney NSW, Australia – name: 3 UT D Anderson Cancer Center, Department of Plastic Surgery, Houston, TX 77030, USA – name: 1 Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston, TX 77030, USA |
Author_xml | – sequence: 1 givenname: Alexander M. surname: Saucedo fullname: Saucedo, Alexander M. organization: Michael E. DeBakey Department of Surgery, Baylor College of Medicine – sequence: 2 givenname: Jorge surname: De La Cerda fullname: De La Cerda, Jorge organization: Small Animal Imaging Resource, UT MD Anderson Cancer Center – sequence: 3 givenname: Hiroo surname: Suami fullname: Suami, Hiroo organization: Department of Plastic Surgery, UT MD Anderson Cancer Center, Medicine and Health Sciences, Macquarie University – sequence: 4 givenname: Rita E. surname: Serda fullname: Serda, Rita E. email: rserda@salud.unm.edu organization: Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Department of Nanomedicine, Houston Methodist, Molecular Medicine, Internal Medicine, University of New Mexico Health Science Center |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30535532$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1016_j_isci_2020_101807 crossref_primary_10_1016_j_apsb_2019_06_011 crossref_primary_10_3390_pharmaceutics14020382 crossref_primary_10_1126_sciadv_aba6156 crossref_primary_10_3390_cancers13123008 |
Cites_doi | 10.1007/s13193-016-0512-6 10.5483/BMBRep.2013.46.3.036 10.1002/nbm.3111 10.1073/pnas.1424024112 10.1006/scbi.2000.0361 10.1038/srep10178 10.1182/blood-2014-05-552729 10.1016/S1359-6446(03)02686-2 10.1038/bjc.2016.172 10.1016/j.jtbi.2007.09.031 10.1053/sonc.2002.37265 10.1371/journal.pone.0027690 10.1007/978-3-319-53156-4_8 10.1158/1078-0432.CCR-14-0493 10.1186/s13054-017-1678-1 10.1097/IGC.0b013e3182a80a41 |
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Title | Multimodal imaging of the tumor microenvironment and biological responses to immune therapy |
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