CD8+ T cells inhibit metastasis and CXCL4 regulates its function
Background The mechanism by which immune cells regulate metastasis is unclear. Understanding the role of immune cells in metastasis will guide the development of treatments improving patient survival. Methods We used syngeneic orthotopic mouse tumour models (wild-type, NOD/scid and Nude), employed k...
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| Published in | British journal of cancer Vol. 125; no. 2; pp. 176 - 189 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
20.07.2021
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0007-0920 1532-1827 1532-1827 |
| DOI | 10.1038/s41416-021-01338-5 |
Cover
| Abstract | Background
The mechanism by which immune cells regulate metastasis is unclear. Understanding the role of immune cells in metastasis will guide the development of treatments improving patient survival.
Methods
We used syngeneic orthotopic mouse tumour models (wild-type, NOD/scid and Nude), employed knockout (
CD8
and
CD4
) models and administered CXCL4. Tumours and lungs were analysed for cancer cells by bioluminescence, and circulating tumour cells were isolated from blood. Immunohistochemistry on the mouse tumours was performed to confirm cell type, and on a tissue microarray with 180 TNBCs for human relevance. TCGA data from over 10,000 patients were analysed as well.
Results
We reveal that intratumoral immune infiltration differs between metastatic and non-metastatic tumours. The non-metastatic tumours harbour high levels of CD8
+
T cells and low levels of platelets, which is reverse in metastatic tumours. During tumour progression, platelets and CXCL4 induce differentiation of monocytes into myeloid-derived suppressor cells (MDSCs), which inhibit CD8
+
T-cell function. TCGA pan-cancer data confirmed that CD8
low
Platelet
high
patients have a significantly lower survival probability compared to CD8
high
Platelet
low
.
Conclusions
CD8
+
T cells inhibit metastasis. When the balance between CD8
+
T cells and platelets is disrupted, platelets produce CXCL4, which induces MDSCs thereby inhibiting the CD8
+
T-cell function. |
|---|---|
| AbstractList | The mechanism by which immune cells regulate metastasis is unclear. Understanding the role of immune cells in metastasis will guide the development of treatments improving patient survival.
We used syngeneic orthotopic mouse tumour models (wild-type, NOD/scid and Nude), employed knockout (CD8 and CD4) models and administered CXCL4. Tumours and lungs were analysed for cancer cells by bioluminescence, and circulating tumour cells were isolated from blood. Immunohistochemistry on the mouse tumours was performed to confirm cell type, and on a tissue microarray with 180 TNBCs for human relevance. TCGA data from over 10,000 patients were analysed as well.
We reveal that intratumoral immune infiltration differs between metastatic and non-metastatic tumours. The non-metastatic tumours harbour high levels of CD8
T cells and low levels of platelets, which is reverse in metastatic tumours. During tumour progression, platelets and CXCL4 induce differentiation of monocytes into myeloid-derived suppressor cells (MDSCs), which inhibit CD8
T-cell function. TCGA pan-cancer data confirmed that CD8
Platelet
patients have a significantly lower survival probability compared to CD8
Platelet
.
CD8
T cells inhibit metastasis. When the balance between CD8
T cells and platelets is disrupted, platelets produce CXCL4, which induces MDSCs thereby inhibiting the CD8
T-cell function. BackgroundThe mechanism by which immune cells regulate metastasis is unclear. Understanding the role of immune cells in metastasis will guide the development of treatments improving patient survival.MethodsWe used syngeneic orthotopic mouse tumour models (wild-type, NOD/scid and Nude), employed knockout (CD8 and CD4) models and administered CXCL4. Tumours and lungs were analysed for cancer cells by bioluminescence, and circulating tumour cells were isolated from blood. Immunohistochemistry on the mouse tumours was performed to confirm cell type, and on a tissue microarray with 180 TNBCs for human relevance. TCGA data from over 10,000 patients were analysed as well.ResultsWe reveal that intratumoral immune infiltration differs between metastatic and non-metastatic tumours. The non-metastatic tumours harbour high levels of CD8+ T cells and low levels of platelets, which is reverse in metastatic tumours. During tumour progression, platelets and CXCL4 induce differentiation of monocytes into myeloid-derived suppressor cells (MDSCs), which inhibit CD8+ T-cell function. TCGA pan-cancer data confirmed that CD8lowPlatelethigh patients have a significantly lower survival probability compared to CD8highPlateletlow.ConclusionsCD8+ T cells inhibit metastasis. When the balance between CD8+ T cells and platelets is disrupted, platelets produce CXCL4, which induces MDSCs thereby inhibiting the CD8+ T-cell function. The mechanism by which immune cells regulate metastasis is unclear. Understanding the role of immune cells in metastasis will guide the development of treatments improving patient survival.BACKGROUNDThe mechanism by which immune cells regulate metastasis is unclear. Understanding the role of immune cells in metastasis will guide the development of treatments improving patient survival.We used syngeneic orthotopic mouse tumour models (wild-type, NOD/scid and Nude), employed knockout (CD8 and CD4) models and administered CXCL4. Tumours and lungs were analysed for cancer cells by bioluminescence, and circulating tumour cells were isolated from blood. Immunohistochemistry on the mouse tumours was performed to confirm cell type, and on a tissue microarray with 180 TNBCs for human relevance. TCGA data from over 10,000 patients were analysed as well.METHODSWe used syngeneic orthotopic mouse tumour models (wild-type, NOD/scid and Nude), employed knockout (CD8 and CD4) models and administered CXCL4. Tumours and lungs were analysed for cancer cells by bioluminescence, and circulating tumour cells were isolated from blood. Immunohistochemistry on the mouse tumours was performed to confirm cell type, and on a tissue microarray with 180 TNBCs for human relevance. TCGA data from over 10,000 patients were analysed as well.We reveal that intratumoral immune infiltration differs between metastatic and non-metastatic tumours. The non-metastatic tumours harbour high levels of CD8+ T cells and low levels of platelets, which is reverse in metastatic tumours. During tumour progression, platelets and CXCL4 induce differentiation of monocytes into myeloid-derived suppressor cells (MDSCs), which inhibit CD8+ T-cell function. TCGA pan-cancer data confirmed that CD8lowPlatelethigh patients have a significantly lower survival probability compared to CD8highPlateletlow.RESULTSWe reveal that intratumoral immune infiltration differs between metastatic and non-metastatic tumours. The non-metastatic tumours harbour high levels of CD8+ T cells and low levels of platelets, which is reverse in metastatic tumours. During tumour progression, platelets and CXCL4 induce differentiation of monocytes into myeloid-derived suppressor cells (MDSCs), which inhibit CD8+ T-cell function. TCGA pan-cancer data confirmed that CD8lowPlatelethigh patients have a significantly lower survival probability compared to CD8highPlateletlow.CD8+ T cells inhibit metastasis. When the balance between CD8+ T cells and platelets is disrupted, platelets produce CXCL4, which induces MDSCs thereby inhibiting the CD8+ T-cell function.CONCLUSIONSCD8+ T cells inhibit metastasis. When the balance between CD8+ T cells and platelets is disrupted, platelets produce CXCL4, which induces MDSCs thereby inhibiting the CD8+ T-cell function. Background The mechanism by which immune cells regulate metastasis is unclear. Understanding the role of immune cells in metastasis will guide the development of treatments improving patient survival. Methods We used syngeneic orthotopic mouse tumour models (wild-type, NOD/scid and Nude), employed knockout ( CD8 and CD4 ) models and administered CXCL4. Tumours and lungs were analysed for cancer cells by bioluminescence, and circulating tumour cells were isolated from blood. Immunohistochemistry on the mouse tumours was performed to confirm cell type, and on a tissue microarray with 180 TNBCs for human relevance. TCGA data from over 10,000 patients were analysed as well. Results We reveal that intratumoral immune infiltration differs between metastatic and non-metastatic tumours. The non-metastatic tumours harbour high levels of CD8 + T cells and low levels of platelets, which is reverse in metastatic tumours. During tumour progression, platelets and CXCL4 induce differentiation of monocytes into myeloid-derived suppressor cells (MDSCs), which inhibit CD8 + T-cell function. TCGA pan-cancer data confirmed that CD8 low Platelet high patients have a significantly lower survival probability compared to CD8 high Platelet low . Conclusions CD8 + T cells inhibit metastasis. When the balance between CD8 + T cells and platelets is disrupted, platelets produce CXCL4, which induces MDSCs thereby inhibiting the CD8 + T-cell function. |
| Author | Tian, Lin Mani, Sendurai A. Acharya, Ghanashyam Soundararajan, Rama Rosen, Jeffrey M. Sahin, Aysegul A. Haemmerle, Monika Allton, Kendra L. Joseph, Robiya Solis, Luisa M. Wistuba, Ignacio I. Shin, Crystal Gibbons, Don L. Barton, Michelle C. Chang, Jeffrey T. Varadarajan, Navin Zhou, Tieling Sood, Anil K. Vasaikar, Suhas Mino, Barbara Martinez-Paniagua, Melisa Rodriguez-Canales, Jaime Isgandarova, Sevinj den Hollander, Petra Yang, Fei Gelovani, Juri Zhang, Xiang H. |
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Tian fullname: Tian, Lin organization: Department of Molecular and Cellular Biology, Baylor College of Medicine, Sloan Kettering Institute – sequence: 7 givenname: Petra surname: den Hollander fullname: den Hollander, Petra organization: Department of Translational Molecular Pathology, The University of Texas MD Anderson Cancer Center – sequence: 8 givenname: Sevinj surname: Isgandarova fullname: Isgandarova, Sevinj organization: Institute of Biosciences and Technology, Texas A&M Health Science Center – sequence: 9 givenname: Monika surname: Haemmerle fullname: Haemmerle, Monika organization: Department of Gynecologic Oncology and Reproductive Medicine and Cancer Biology, The University of Texas MD Anderson Cancer Center, University Clinic Halle, Institute of Pathology – sequence: 10 givenname: Barbara surname: Mino fullname: Mino, Barbara organization: Department of Translational Molecular Pathology, The University of Texas MD Anderson Cancer Center – sequence: 11 givenname: Tieling surname: Zhou fullname: Zhou, Tieling organization: Department of Translational Molecular Pathology, The University of Texas MD Anderson Cancer Center – sequence: 12 givenname: Crystal surname: Shin fullname: Shin, Crystal organization: Department of Surgery, Baylor College of Medicine – sequence: 13 givenname: Melisa surname: Martinez-Paniagua fullname: Martinez-Paniagua, Melisa organization: Department of Chemical and Biomolecular Engineering, University of Houston – sequence: 14 givenname: Aysegul A. surname: Sahin fullname: Sahin, Aysegul A. organization: Department of Pathology, Division of Pathology/Lab Medicine, The University of Texas MD Anderson Cancer Center – sequence: 15 givenname: Jaime surname: Rodriguez-Canales fullname: Rodriguez-Canales, Jaime organization: Department of Translational Molecular Pathology, The University of Texas MD Anderson Cancer Center, AstraZeneca – sequence: 16 givenname: Juri surname: Gelovani fullname: Gelovani, Juri organization: Department of Experimental Diagnostic Imaging, Wayne State University – sequence: 17 givenname: Jeffrey T. surname: Chang fullname: Chang, Jeffrey T. organization: Department of Integrative Biology and Pharmacology, UT Health Sciences Center at Houston – sequence: 18 givenname: Ghanashyam surname: Acharya fullname: Acharya, Ghanashyam organization: Department of Surgery, Baylor College of Medicine – sequence: 19 givenname: Anil K. surname: Sood fullname: Sood, Anil K. organization: Department of Gynecologic Oncology and Reproductive Medicine and Cancer Biology, The University of Texas MD Anderson Cancer Center – sequence: 20 givenname: Ignacio I. surname: Wistuba fullname: Wistuba, Ignacio I. organization: Department of Translational Molecular Pathology, The University of Texas MD Anderson Cancer Center – sequence: 21 givenname: Don L. orcidid: 0000-0003-2362-3094 surname: Gibbons fullname: Gibbons, Don L. organization: Department of Thoracic Head and Neck Medical Oncology, Division of Cancer Medicine Division, The University of Texas MD Anderson Cancer Center – sequence: 22 givenname: Luisa M. surname: Solis fullname: Solis, Luisa M. organization: Department of Translational Molecular Pathology, The University of Texas MD Anderson Cancer Center – sequence: 23 givenname: Michelle C. surname: Barton fullname: Barton, Michelle C. organization: Department of Epigenetics and Molecular Carcinogenesis, The University of Texas MD Anderson Cancer Center – sequence: 24 givenname: Navin surname: Varadarajan fullname: Varadarajan, Navin organization: Department of Chemical and Biomolecular Engineering, University of Houston – sequence: 25 givenname: Jeffrey M. surname: Rosen fullname: Rosen, Jeffrey M. organization: Department of Molecular and Cellular Biology, Baylor College of Medicine – sequence: 26 givenname: Xiang H. surname: Zhang fullname: Zhang, Xiang H. organization: Department of Molecular and Cellular Biology, Baylor College of Medicine – sequence: 27 givenname: Sendurai A. orcidid: 0000-0002-5918-4276 surname: Mani fullname: Mani, Sendurai A. email: smani@mdanderson.org organization: Department of Translational Molecular Pathology, The University of Texas MD Anderson Cancer Center |
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| PublicationPlace_xml | – name: London – name: England |
| PublicationTitle | British journal of cancer |
| PublicationTitleAbbrev | Br J Cancer |
| PublicationTitleAlternate | Br J Cancer |
| PublicationYear | 2021 |
| Publisher | Nature Publishing Group UK Nature Publishing Group |
| Publisher_xml | – name: Nature Publishing Group UK – name: Nature Publishing Group |
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The mechanism by which immune cells regulate metastasis is unclear. Understanding the role of immune cells in metastasis will guide the development... The mechanism by which immune cells regulate metastasis is unclear. Understanding the role of immune cells in metastasis will guide the development of... BackgroundThe mechanism by which immune cells regulate metastasis is unclear. Understanding the role of immune cells in metastasis will guide the development... |
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| Title | CD8+ T cells inhibit metastasis and CXCL4 regulates its function |
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