Stromal cell diversity associated with immune evasion in human triple‐negative breast cancer
The tumour stroma regulates nearly all stages of carcinogenesis. Stromal heterogeneity in human triple‐negative breast cancers (TNBCs) remains poorly understood, limiting the development of stromal‐targeted therapies. Single‐cell RNA sequencing of five TNBCs revealed two cancer‐associated fibroblast...
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| Vydáno v: | The EMBO journal Ročník 39; číslo 19; s. e104063 - n/a |
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| Hlavní autoři: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
| Vydáno: |
London
Nature Publishing Group UK
01.10.2020
Springer Nature B.V John Wiley and Sons Inc |
| Témata: | |
| ISSN: | 0261-4189, 1460-2075, 1460-2075 |
| On-line přístup: | Získat plný text |
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| Abstract | The tumour stroma regulates nearly all stages of carcinogenesis. Stromal heterogeneity in human triple‐negative breast cancers (TNBCs) remains poorly understood, limiting the development of stromal‐targeted therapies. Single‐cell RNA sequencing of five TNBCs revealed two cancer‐associated fibroblast (CAF) and two perivascular‐like (PVL) subpopulations. CAFs clustered into two states: the first with features of myofibroblasts and the second characterised by high expression of growth factors and immunomodulatory molecules. PVL cells clustered into two states consistent with a differentiated and immature phenotype. We showed that these stromal states have distinct morphologies, spatial relationships and functional properties in regulating the extracellular matrix. Using cell signalling predictions, we provide evidence that stromal‐immune crosstalk acts
via
a diverse array of immunoregulatory molecules. Importantly, the investigation of gene signatures from inflammatory‐CAFs and differentiated‐PVL cells in independent TNBC patient cohorts revealed strong associations with cytotoxic T‐cell dysfunction and exclusion, respectively. Such insights present promising candidates to further investigate for new therapeutic strategies in the treatment of TNBCs.
Synopsis
This single‐cell gene expression resource deciphers the composition of triple‐negative breast cancer (TNBC) stroma, revealing distinct subclasses of cancer‐associated fibroblasts (CAFs) and perivascular‐like (PVL) cells. These signatures are informative on tumour aetiology and potential strategies for development of targeted therapies.
Single‐cell analysis of primary TNBC highlights clusters of stromal and immune cell types.
TNBC stroma is comprised of myofibroblast‐like CAFs, inflammatory‐like CAFs, differentiated PVL and immature PVL cells.
Stromal subclasses differ in surface markers, spatial localisation in tissue, ECM functions, and predicted cellular crosstalk with immune cells.
Inflammatory‐like CAF and differentiated PVL cells are associated with cytotoxic T‐cell dysfunction and exclusion in independent TNBC‐patient cohorts.
Graphical Abstract
Single‐cell profiling of primary breast cancer provides unprecedented insights into cell‐type heterogeneity within the tumor microenvironment. |
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| AbstractList | The tumour stroma regulates nearly all stages of carcinogenesis. Stromal heterogeneity in human triple‐negative breast cancers (TNBCs) remains poorly understood, limiting the development of stromal‐targeted therapies. Single‐cell RNA sequencing of five TNBCs revealed two cancer‐associated fibroblast (CAF) and two perivascular‐like (PVL) subpopulations. CAFs clustered into two states: the first with features of myofibroblasts and the second characterised by high expression of growth factors and immunomodulatory molecules. PVL cells clustered into two states consistent with a differentiated and immature phenotype. We showed that these stromal states have distinct morphologies, spatial relationships and functional properties in regulating the extracellular matrix. Using cell signalling predictions, we provide evidence that stromal‐immune crosstalk acts via a diverse array of immunoregulatory molecules. Importantly, the investigation of gene signatures from inflammatory‐CAFs and differentiated‐PVL cells in independent TNBC patient cohorts revealed strong associations with cytotoxic T‐cell dysfunction and exclusion, respectively. Such insights present promising candidates to further investigate for new therapeutic strategies in the treatment of TNBCs. Single‐cell profiling of primary breast cancer provides unprecedented insights into cell‐type heterogeneity within the tumor microenvironment. The tumour stroma regulates nearly all stages of carcinogenesis. Stromal heterogeneity in human triple-negative breast cancers (TNBCs) remains poorly understood, limiting the development of stromal-targeted therapies. Single-cell RNA sequencing of five TNBCs revealed two cancer-associated fibroblast (CAF) and two perivascular-like (PVL) subpopulations. CAFs clustered into two states: the first with features of myofibroblasts and the second characterised by high expression of growth factors and immunomodulatory molecules. PVL cells clustered into two states consistent with a differentiated and immature phenotype. We showed that these stromal states have distinct morphologies, spatial relationships and functional properties in regulating the extracellular matrix. Using cell signalling predictions, we provide evidence that stromal-immune crosstalk acts via a diverse array of immunoregulatory molecules. Importantly, the investigation of gene signatures from inflammatory-CAFs and differentiated-PVL cells in independent TNBC patient cohorts revealed strong associations with cytotoxic T-cell dysfunction and exclusion, respectively. Such insights present promising candidates to further investigate for new therapeutic strategies in the treatment of TNBCs. The tumour stroma regulates nearly all stages of carcinogenesis. Stromal heterogeneity in human triple‐negative breast cancers (TNBCs) remains poorly understood, limiting the development of stromal‐targeted therapies. Single‐cell RNA sequencing of five TNBCs revealed two cancer‐associated fibroblast (CAF) and two perivascular‐like (PVL) subpopulations. CAFs clustered into two states: the first with features of myofibroblasts and the second characterised by high expression of growth factors and immunomodulatory molecules. PVL cells clustered into two states consistent with a differentiated and immature phenotype. We showed that these stromal states have distinct morphologies, spatial relationships and functional properties in regulating the extracellular matrix. Using cell signalling predictions, we provide evidence that stromal‐immune crosstalk acts via a diverse array of immunoregulatory molecules. Importantly, the investigation of gene signatures from inflammatory‐CAFs and differentiated‐PVL cells in independent TNBC patient cohorts revealed strong associations with cytotoxic T‐cell dysfunction and exclusion, respectively. Such insights present promising candidates to further investigate for new therapeutic strategies in the treatment of TNBCs. Synopsis This single‐cell gene expression resource deciphers the composition of triple‐negative breast cancer (TNBC) stroma, revealing distinct subclasses of cancer‐associated fibroblasts (CAFs) and perivascular‐like (PVL) cells. These signatures are informative on tumour aetiology and potential strategies for development of targeted therapies. Single‐cell analysis of primary TNBC highlights clusters of stromal and immune cell types. TNBC stroma is comprised of myofibroblast‐like CAFs, inflammatory‐like CAFs, differentiated PVL and immature PVL cells. Stromal subclasses differ in surface markers, spatial localisation in tissue, ECM functions, and predicted cellular crosstalk with immune cells. Inflammatory‐like CAF and differentiated PVL cells are associated with cytotoxic T‐cell dysfunction and exclusion in independent TNBC‐patient cohorts. Graphical Abstract Single‐cell profiling of primary breast cancer provides unprecedented insights into cell‐type heterogeneity within the tumor microenvironment. The tumour stroma regulates nearly all stages of carcinogenesis. Stromal heterogeneity in human triple-negative breast cancers (TNBCs) remains poorly understood, limiting the development of stromal-targeted therapies. Single-cell RNA sequencing of five TNBCs revealed two cancer-associated fibroblast (CAF) and two perivascular-like (PVL) subpopulations. CAFs clustered into two states: the first with features of myofibroblasts and the second characterised by high expression of growth factors and immunomodulatory molecules. PVL cells clustered into two states consistent with a differentiated and immature phenotype. We showed that these stromal states have distinct morphologies, spatial relationships and functional properties in regulating the extracellular matrix. Using cell signalling predictions, we provide evidence that stromal-immune crosstalk acts via a diverse array of immunoregulatory molecules. Importantly, the investigation of gene signatures from inflammatory-CAFs and differentiated-PVL cells in independent TNBC patient cohorts revealed strong associations with cytotoxic T-cell dysfunction and exclusion, respectively. Such insights present promising candidates to further investigate for new therapeutic strategies in the treatment of TNBCs.The tumour stroma regulates nearly all stages of carcinogenesis. Stromal heterogeneity in human triple-negative breast cancers (TNBCs) remains poorly understood, limiting the development of stromal-targeted therapies. Single-cell RNA sequencing of five TNBCs revealed two cancer-associated fibroblast (CAF) and two perivascular-like (PVL) subpopulations. CAFs clustered into two states: the first with features of myofibroblasts and the second characterised by high expression of growth factors and immunomodulatory molecules. PVL cells clustered into two states consistent with a differentiated and immature phenotype. We showed that these stromal states have distinct morphologies, spatial relationships and functional properties in regulating the extracellular matrix. Using cell signalling predictions, we provide evidence that stromal-immune crosstalk acts via a diverse array of immunoregulatory molecules. Importantly, the investigation of gene signatures from inflammatory-CAFs and differentiated-PVL cells in independent TNBC patient cohorts revealed strong associations with cytotoxic T-cell dysfunction and exclusion, respectively. Such insights present promising candidates to further investigate for new therapeutic strategies in the treatment of TNBCs. The tumour stroma regulates nearly all stages of carcinogenesis. Stromal heterogeneity in human triple‐negative breast cancers (TNBCs) remains poorly understood, limiting the development of stromal‐targeted therapies. Single‐cell RNA sequencing of five TNBCs revealed two cancer‐associated fibroblast (CAF) and two perivascular‐like (PVL) subpopulations. CAFs clustered into two states: the first with features of myofibroblasts and the second characterised by high expression of growth factors and immunomodulatory molecules. PVL cells clustered into two states consistent with a differentiated and immature phenotype. We showed that these stromal states have distinct morphologies, spatial relationships and functional properties in regulating the extracellular matrix. Using cell signalling predictions, we provide evidence that stromal‐immune crosstalk acts via a diverse array of immunoregulatory molecules. Importantly, the investigation of gene signatures from inflammatory‐CAFs and differentiated‐PVL cells in independent TNBC patient cohorts revealed strong associations with cytotoxic T‐cell dysfunction and exclusion, respectively. Such insights present promising candidates to further investigate for new therapeutic strategies in the treatment of TNBCs. Synopsis This single‐cell gene expression resource deciphers the composition of triple‐negative breast cancer (TNBC) stroma, revealing distinct subclasses of cancer‐associated fibroblasts (CAFs) and perivascular‐like (PVL) cells. These signatures are informative on tumour aetiology and potential strategies for development of targeted therapies. Single‐cell analysis of primary TNBC highlights clusters of stromal and immune cell types. TNBC stroma is comprised of myofibroblast‐like CAFs, inflammatory‐like CAFs, differentiated PVL and immature PVL cells. Stromal subclasses differ in surface markers, spatial localisation in tissue, ECM functions, and predicted cellular crosstalk with immune cells. Inflammatory‐like CAF and differentiated PVL cells are associated with cytotoxic T‐cell dysfunction and exclusion in independent TNBC‐patient cohorts. Single‐cell profiling of primary breast cancer provides unprecedented insights into cell‐type heterogeneity within the tumor microenvironment. |
| Author | Forrest, Alistair Robbins, Elizabeth Torpy, James R Mak, Cindy Cox, Thomas R Lim, Elgene Bartonicek, Nenad Parker, Andrew Liu, X Shirley Chan, Chia‐Ling Murphy, Kendelle J Powell, Joseph Roden, Daniel L Holliday, Holly Hou, Rui Beith, Jane Lam, Chuan En Cooper, Caroline Junankar, Simon Timpson, Paul Al‐Eryani, Ghamdan Wang, Chenfei Pereira, Brooke Cazet, Aurélie S O'Toole, Sandra Harvey, Kate Swarbrick, Alexander Hui, Mun N Gluch, Laurence Warrier, Sanjay Segara, Davendra Wu, Sunny Z |
| AuthorAffiliation | 8 St Vincent's Hospital Darlinghurst NSW Australia 3 Department of Data Sciences Center for Functional Cancer Epigenetics Dana‐Farber Cancer Institute Harvard T.H. Chan School of Public Health Boston MA USA 11 Southside Clinical Unit Faculty of Medicine University of Queensland Brisbane Qld Australia 12 Department of Breast Surgery Chris O'Brien Lifehouse Camperdown NSW Australia 16 Australian Clinical Laboratories Northern Beaches Hospital Frenchs Forest NSW Australia 6 Chris O'Brien Lifehouse Camperdown NSW Australia 15 UNSW Cellular Genomics Futures Institute University of New South Wales Sydney NSW Australia 13 Royal Prince Alfred Institute of Academic Surgery Sydney University Sydney NSW Australia 7 The Strathfield Breast Centre Strathfield NSW Australia 2 St Vincent's Clinical School Faculty of Medicine UNSW Sydney Sydney NSW Australia 5 Garvan‐Weizmann Centre for Cellular Genomics Garvan Institute of Medical Research Sydney NSW Australia 14 RIKEN Center for Integrative Medical Sciences Yok |
| AuthorAffiliation_xml | – name: 12 Department of Breast Surgery Chris O'Brien Lifehouse Camperdown NSW Australia – name: 15 UNSW Cellular Genomics Futures Institute University of New South Wales Sydney NSW Australia – name: 2 St Vincent's Clinical School Faculty of Medicine UNSW Sydney Sydney NSW Australia – name: 10 Pathology Queensland Princess Alexandra Hospital Brisbane Qld Australia – name: 13 Royal Prince Alfred Institute of Academic Surgery Sydney University Sydney NSW Australia – name: 16 Australian Clinical Laboratories Northern Beaches Hospital Frenchs Forest NSW Australia – name: 3 Department of Data Sciences Center for Functional Cancer Epigenetics Dana‐Farber Cancer Institute Harvard T.H. Chan School of Public Health Boston MA USA – name: 6 Chris O'Brien Lifehouse Camperdown NSW Australia – name: 7 The Strathfield Breast Centre Strathfield NSW Australia – name: 14 RIKEN Center for Integrative Medical Sciences Yokohama Japan – name: 11 Southside Clinical Unit Faculty of Medicine University of Queensland Brisbane Qld Australia – name: 4 Harry Perkins Institute of Medical Research QEII Medical Centre and Centre for Medical Research The University of Western Australia Nedlands, Perth WA Australia – name: 8 St Vincent's Hospital Darlinghurst NSW Australia – name: 5 Garvan‐Weizmann Centre for Cellular Genomics Garvan Institute of Medical Research Sydney NSW Australia – name: 1 The Kinghorn Cancer Centre and Cancer Research Division Garvan Institute of Medical Research Darlinghurst NSW Australia – name: 9 Royal Prince Alfred Hospital Camperdown NSW Australia |
| Author_xml | – sequence: 1 givenname: Sunny Z surname: Wu fullname: Wu, Sunny Z organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney – sequence: 2 givenname: Daniel L surname: Roden fullname: Roden, Daniel L organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney – sequence: 3 givenname: Chenfei surname: Wang fullname: Wang, Chenfei organization: Department of Data Sciences, Center for Functional Cancer Epigenetics, Dana‐Farber Cancer Institute, Harvard T.H. Chan School of Public Health – sequence: 4 givenname: Holly surname: Holliday fullname: Holliday, Holly organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney – sequence: 5 givenname: Kate surname: Harvey fullname: Harvey, Kate organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research – sequence: 6 givenname: Aurélie S surname: Cazet fullname: Cazet, Aurélie S organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney – sequence: 7 givenname: Kendelle J surname: Murphy fullname: Murphy, Kendelle J organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney – sequence: 8 givenname: Brooke surname: Pereira fullname: Pereira, Brooke organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney – sequence: 9 givenname: Ghamdan surname: Al‐Eryani fullname: Al‐Eryani, Ghamdan organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney – sequence: 10 givenname: Nenad surname: Bartonicek fullname: Bartonicek, Nenad organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney – sequence: 11 givenname: Rui surname: Hou fullname: Hou, Rui organization: Harry Perkins Institute of Medical Research, QEII Medical Centre and Centre for Medical Research, The University of Western Australia – sequence: 12 givenname: James R surname: Torpy fullname: Torpy, James R organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney – sequence: 13 givenname: Simon surname: Junankar fullname: Junankar, Simon organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney – sequence: 14 givenname: Chia‐Ling surname: Chan fullname: Chan, Chia‐Ling organization: Garvan‐Weizmann Centre for Cellular Genomics, Garvan Institute of Medical Research – sequence: 15 givenname: Chuan En surname: Lam fullname: Lam, Chuan En organization: Garvan‐Weizmann Centre for Cellular Genomics, Garvan Institute of Medical Research – sequence: 16 givenname: Mun N surname: Hui fullname: Hui, Mun N organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, Chris O'Brien Lifehouse – sequence: 17 givenname: Laurence surname: Gluch fullname: Gluch, Laurence organization: The Strathfield Breast Centre – sequence: 18 givenname: Jane surname: Beith fullname: Beith, Jane organization: Chris O'Brien Lifehouse – sequence: 19 givenname: Andrew surname: Parker fullname: Parker, Andrew organization: St Vincent's Hospital – sequence: 20 givenname: Elizabeth surname: Robbins fullname: Robbins, Elizabeth organization: Royal Prince Alfred Hospital – sequence: 21 givenname: Davendra surname: Segara fullname: Segara, Davendra organization: St Vincent's Hospital – sequence: 22 givenname: Cindy surname: Mak fullname: Mak, Cindy organization: Chris O'Brien Lifehouse – sequence: 23 givenname: Caroline surname: Cooper fullname: Cooper, Caroline organization: Pathology Queensland, Princess Alexandra Hospital, Southside Clinical Unit, Faculty of Medicine, University of Queensland – sequence: 24 givenname: Sanjay surname: Warrier fullname: Warrier, Sanjay organization: Department of Breast Surgery, Chris O'Brien Lifehouse, Royal Prince Alfred Institute of Academic Surgery, Sydney University – sequence: 25 givenname: Alistair surname: Forrest fullname: Forrest, Alistair organization: Harry Perkins Institute of Medical Research, QEII Medical Centre and Centre for Medical Research, The University of Western Australia, RIKEN Center for Integrative Medical Sciences – sequence: 26 givenname: Joseph surname: Powell fullname: Powell, Joseph organization: Garvan‐Weizmann Centre for Cellular Genomics, Garvan Institute of Medical Research, UNSW Cellular Genomics Futures Institute, University of New South Wales – sequence: 27 givenname: Sandra surname: O'Toole fullname: O'Toole, Sandra organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney, Australian Clinical Laboratories, Northern Beaches Hospital – sequence: 28 givenname: Thomas R orcidid: 0000-0001-9294-1745 surname: Cox fullname: Cox, Thomas R organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney – sequence: 29 givenname: Paul surname: Timpson fullname: Timpson, Paul organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney – sequence: 30 givenname: Elgene surname: Lim fullname: Lim, Elgene organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney, St Vincent's Hospital – sequence: 31 givenname: X Shirley surname: Liu fullname: Liu, X Shirley organization: Department of Data Sciences, Center for Functional Cancer Epigenetics, Dana‐Farber Cancer Institute, Harvard T.H. Chan School of Public Health – sequence: 32 givenname: Alexander orcidid: 0000-0002-3051-5676 surname: Swarbrick fullname: Swarbrick, Alexander email: a.swarbrick@garvan.org.au organization: The Kinghorn Cancer Centre and Cancer Research Division, Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, UNSW Sydney |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32790115$$D View this record in MEDLINE/PubMed |
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| Snippet | The tumour stroma regulates nearly all stages of carcinogenesis. Stromal heterogeneity in human triple‐negative breast cancers (TNBCs) remains poorly... The tumour stroma regulates nearly all stages of carcinogenesis. Stromal heterogeneity in human triple-negative breast cancers (TNBCs) remains poorly... |
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| SubjectTerms | Breast cancer cancer‐associated fibroblasts Carcinogenesis Carcinogens Cell differentiation Crosstalk Cytotoxicity Development strategies EMBO03 EMBO19 Extracellular matrix Extracellular Matrix - immunology Extracellular Matrix - pathology Female Fibroblasts Gene expression Gene sequencing Growth factors Heterogeneity Humans Immune evasion Immune system Immunomodulation Immunomodulators Immunoregulation Inflammation Phenotypes Resource Ribonucleic acid RNA RNA-Seq Signatures single‐cell RNA sequencing Stromal Cells - immunology Stromal Cells - pathology stromal heterogeneity Subpopulations Surface markers T-Lymphocytes, Cytotoxic - immunology T-Lymphocytes, Cytotoxic - pathology Triple Negative Breast Neoplasms - immunology Triple Negative Breast Neoplasms - pathology triple‐negative breast cancer Tumor Escape Tumors tumour microenvironment |
| Title | Stromal cell diversity associated with immune evasion in human triple‐negative breast cancer |
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