Organoid Modeling of the Tumor Immune Microenvironment
In vitro cancer cultures, including three-dimensional organoids, typically contain exclusively neoplastic epithelium but require artificial reconstitution to recapitulate the tumor microenvironment (TME). The co-culture of primary tumor epithelia with endogenous, syngeneic tumor-infiltrating lymphoc...
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| Published in | Cell Vol. 175; no. 7; pp. 1972 - 1988.e16 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
13.12.2018
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0092-8674 1097-4172 1097-4172 |
| DOI | 10.1016/j.cell.2018.11.021 |
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| Abstract | In vitro cancer cultures, including three-dimensional organoids, typically contain exclusively neoplastic epithelium but require artificial reconstitution to recapitulate the tumor microenvironment (TME). The co-culture of primary tumor epithelia with endogenous, syngeneic tumor-infiltrating lymphocytes (TILs) as a cohesive unit has been particularly elusive. Here, an air-liquid interface (ALI) method propagated patient-derived organoids (PDOs) from >100 human biopsies or mouse tumors in syngeneic immunocompetent hosts as tumor epithelia with native embedded immune cells (T, B, NK, macrophages). Robust droplet-based, single-cell simultaneous determination of gene expression and immune repertoire indicated that PDO TILs accurately preserved the original tumor T cell receptor (TCR) spectrum. Crucially, human and murine PDOs successfully modeled immune checkpoint blockade (ICB) with anti-PD-1- and/or anti-PD-L1 expanding and activating tumor antigen-specific TILs and eliciting tumor cytotoxicity. Organoid-based propagation of primary tumor epithelium en bloc with endogenous immune stroma should enable immuno-oncology investigations within the TME and facilitate personalized immunotherapy testing.
[Display omitted]
•Air-liquid interface (ALI) patient-derived tumor organoids (PDO) retain immune cells•5′ V(D)J and RNA-seq from the same single cells allows robust immune characterization•T cell receptor repertoire is highly conserved between tumor and PDO•ALI PDOs functionally recapitulate the PD-1/PD-L1-dependent immune checkpoint
The tumor-immune microenvironment is modeled using a patient-derived organoid approach that preserves the original tumor T cell receptor spectrum and successfully models immune checkpoint blockade. |
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| AbstractList | In vitro cancer cultures, including 3-dimensional organoids, typically contain exclusively neoplastic epithelium but require artificial reconstitution to recapitulate the tumor microenvironment (TME). The co-culture of primary tumor epithelia with endogenous, syngeneic tumor-infiltrating lymphocytes (TILs) as a cohesive unit has been particularly elusive. Here, an air-liquid interface (ALI) method propagated Patient-Derived Organoids (PDOs) from >100 human biopsies or mouse tumors in syngeneic immunocompetent hosts as tumor epithelia with native embedded immune cells (T, B, NK, macrophages). Robust droplet-based, single cell simultaneous determination of gene expression and immune repertoire indicated that PDO TILs accurately preserved the original tumor T cell receptor (TCR) spectrum. Crucially, human and murine PDOs successfully modeled immune checkpoint blockade (ICB) with anti-PD-1- and/or anti-PD-L1 expanding and activating tumor antigen-specific TILs and eliciting tumor cytotoxicity. Organoid-based propagation of primary tumor epithelium en bloc with endogenous immune stroma should enable immunooncology investigations within the TME and facilitate personalized immunotherapy testing.
The tumor immune microenvironment is modeled using a patient-derived organoid approach that preserves the original tumor T cell receptor spectrum and successfully models immune checkpoint blockade In vitro cancer cultures, including three-dimensional organoids, typically contain exclusively neoplastic epithelium but require artificial reconstitution to recapitulate the tumor microenvironment (TME). The co-culture of primary tumor epithelia with endogenous, syngeneic tumor-infiltrating lymphocytes (TILs) as a cohesive unit has been particularly elusive. Here, an air-liquid interface (ALI) method propagated patient-derived organoids (PDOs) from >100 human biopsies or mouse tumors in syngeneic immunocompetent hosts as tumor epithelia with native embedded immune cells (T, B, NK, macrophages). Robust droplet-based, single-cell simultaneous determination of gene expression and immune repertoire indicated that PDO TILs accurately preserved the original tumor T cell receptor (TCR) spectrum. Crucially, human and murine PDOs successfully modeled immune checkpoint blockade (ICB) with anti-PD-1- and/or anti-PD-L1 expanding and activating tumor antigen-specific TILs and eliciting tumor cytotoxicity. Organoid-based propagation of primary tumor epithelium en bloc with endogenous immune stroma should enable immuno-oncology investigations within the TME and facilitate personalized immunotherapy testing. [Display omitted] •Air-liquid interface (ALI) patient-derived tumor organoids (PDO) retain immune cells•5′ V(D)J and RNA-seq from the same single cells allows robust immune characterization•T cell receptor repertoire is highly conserved between tumor and PDO•ALI PDOs functionally recapitulate the PD-1/PD-L1-dependent immune checkpoint The tumor-immune microenvironment is modeled using a patient-derived organoid approach that preserves the original tumor T cell receptor spectrum and successfully models immune checkpoint blockade. In vitro cancer cultures, including three-dimensional organoids, typically contain exclusively neoplastic epithelium but require artificial reconstitution to recapitulate the tumor microenvironment (TME). The co-culture of primary tumor epithelia with endogenous, syngeneic tumor-infiltrating lymphocytes (TILs) as a cohesive unit has been particularly elusive. Here, an air-liquid interface (ALI) method propagated patient-derived organoids (PDOs) from >100 human biopsies or mouse tumors in syngeneic immunocompetent hosts as tumor epithelia with native embedded immune cells (T, B, NK, macrophages). Robust droplet-based, single-cell simultaneous determination of gene expression and immune repertoire indicated that PDO TILs accurately preserved the original tumor T cell receptor (TCR) spectrum. Crucially, human and murine PDOs successfully modeled immune checkpoint blockade (ICB) with anti-PD-1- and/or anti-PD-L1 expanding and activating tumor antigen-specific TILs and eliciting tumor cytotoxicity. Organoid-based propagation of primary tumor epithelium en bloc with endogenous immune stroma should enable immuno-oncology investigations within the TME and facilitate personalized immunotherapy testing. In vitro cancer cultures, including three-dimensional organoids, typically contain exclusively neoplastic epithelium but require artificial reconstitution to recapitulate the tumor microenvironment (TME). The co-culture of primary tumor epithelia with endogenous, syngeneic tumor-infiltrating lymphocytes (TILs) as a cohesive unit has been particularly elusive. Here, an air-liquid interface (ALI) method propagated patient-derived organoids (PDOs) from >100 human biopsies or mouse tumors in syngeneic immunocompetent hosts as tumor epithelia with native embedded immune cells (T, B, NK, macrophages). Robust droplet-based, single-cell simultaneous determination of gene expression and immune repertoire indicated that PDO TILs accurately preserved the original tumor T cell receptor (TCR) spectrum. Crucially, human and murine PDOs successfully modeled immune checkpoint blockade (ICB) with anti-PD-1- and/or anti-PD-L1 expanding and activating tumor antigen-specific TILs and eliciting tumor cytotoxicity. Organoid-based propagation of primary tumor epithelium en bloc with endogenous immune stroma should enable immuno-oncology investigations within the TME and facilitate personalized immunotherapy testing. In vitro cancer cultures, including three-dimensional organoids, typically contain exclusively neoplastic epithelium but require artificial reconstitution to recapitulate the tumor microenvironment (TME). The co-culture of primary tumor epithelia with endogenous, syngeneic tumor-infiltrating lymphocytes (TILs) as a cohesive unit has been particularly elusive. Here, an air-liquid interface (ALI) method propagated patient-derived organoids (PDOs) from >100 human biopsies or mouse tumors in syngeneic immunocompetent hosts as tumor epithelia with native embedded immune cells (T, B, NK, macrophages). Robust droplet-based, single-cell simultaneous determination of gene expression and immune repertoire indicated that PDO TILs accurately preserved the original tumor T cell receptor (TCR) spectrum. Crucially, human and murine PDOs successfully modeled immune checkpoint blockade (ICB) with anti-PD-1- and/or anti-PD-L1 expanding and activating tumor antigen-specific TILs and eliciting tumor cytotoxicity. Organoid-based propagation of primary tumor epithelium en bloc with endogenous immune stroma should enable immuno-oncology investigations within the TME and facilitate personalized immunotherapy testing.In vitro cancer cultures, including three-dimensional organoids, typically contain exclusively neoplastic epithelium but require artificial reconstitution to recapitulate the tumor microenvironment (TME). The co-culture of primary tumor epithelia with endogenous, syngeneic tumor-infiltrating lymphocytes (TILs) as a cohesive unit has been particularly elusive. Here, an air-liquid interface (ALI) method propagated patient-derived organoids (PDOs) from >100 human biopsies or mouse tumors in syngeneic immunocompetent hosts as tumor epithelia with native embedded immune cells (T, B, NK, macrophages). Robust droplet-based, single-cell simultaneous determination of gene expression and immune repertoire indicated that PDO TILs accurately preserved the original tumor T cell receptor (TCR) spectrum. Crucially, human and murine PDOs successfully modeled immune checkpoint blockade (ICB) with anti-PD-1- and/or anti-PD-L1 expanding and activating tumor antigen-specific TILs and eliciting tumor cytotoxicity. Organoid-based propagation of primary tumor epithelium en bloc with endogenous immune stroma should enable immuno-oncology investigations within the TME and facilitate personalized immunotherapy testing. |
| Author | Tseng, Yuen-Yi Grzeskowiak, Caitlin L. Sabatti, Chiara Zemek, Allison J. De La Vega, Francisco M. Ju, Jihang Mendoza-Villanueva, Daniel Alkhairy, Sahar Kunz, Pamela L. Karlsson, Kasper Neal, James T. Li, Xingnan Salahudeen, Ameen A. Metzner, Thomas J. Chiou, Shin-Heng Giangarra, Valeria Smith, Amber R. Liu, Iris H. Zhao, Fan Liao, Lillian Sunwoo, John B. Oh, Coyin Kuo, Calvin J. Deutsch, Brian C. Boehm, Jesse S. Hahn, William C. Nadauld, Lincoln D. Zheng, Grace X.Y. Liao, Joseph C. Zhu, Junjie Leppert, John T. Schultz, Liora M. Keskula, Paula Davis, Mark M. |
| AuthorAffiliation | 6 Departments of Pathology, Stanford University School of Medicine, Stanford, California, USA 5 Howard Hughes Medical Institute and Department of Microbiology and immunology, Stanford University, Stanford, California, USA 9 Broad Institute of Harvard and MIT, Cambridge, Massachusetts, USA 12 Departments of Biomedical Data Science, Stanford University School of Medicine, Stanford, California, USA 8 Departments of Urology, Stanford University School of Medicine, Stanford, California, USA 15 Current address: Broad Institute of Harvard and MIT, Cambridge, Massachusetts, USA 11 Departments of Otolaryngology, Stanford University School of Medicine, Stanford, California, USA 13 Department of Statistics, Stanford University School of Humanities and Sciences, Stanford, California, USA 7 Department of Oncology, Stanford University School of Medicine, Stanford, California, USA 16 Equal contributions 1 Department of Medicine, Divisions of Hematology, Stanford University School of Medicine, Stanford, Califor |
| AuthorAffiliation_xml | – name: 14 Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, USA – name: 2 Department of Electrical Engineering, Stanford University School of Engineering, Stanford, California, USA – name: 4 Institute for Immunity, Transplantation, and Infection, Stanford University School of Medicine, Stanford, California, USA – name: 1 Department of Medicine, Divisions of Hematology, Stanford University School of Medicine, Stanford, California, USA – name: 8 Departments of Urology, Stanford University School of Medicine, Stanford, California, USA – name: 9 Broad Institute of Harvard and MIT, Cambridge, Massachusetts, USA – name: 13 Department of Statistics, Stanford University School of Humanities and Sciences, Stanford, California, USA – name: 5 Howard Hughes Medical Institute and Department of Microbiology and immunology, Stanford University, Stanford, California, USA – name: 12 Departments of Biomedical Data Science, Stanford University School of Medicine, Stanford, California, USA – name: 15 Current address: Broad Institute of Harvard and MIT, Cambridge, Massachusetts, USA – name: 7 Department of Oncology, Stanford University School of Medicine, Stanford, California, USA – name: 17 Lead contact – name: 3 10x Genomics, Pleasanton, CA – name: 10 TOMA Biosciences, Foster City, California, USA – name: 11 Departments of Otolaryngology, Stanford University School of Medicine, Stanford, California, USA – name: 6 Departments of Pathology, Stanford University School of Medicine, Stanford, California, USA – name: 16 Equal contributions |
| Author_xml | – sequence: 1 givenname: James T. surname: Neal fullname: Neal, James T. organization: Department of Medicine, Division of Hematology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 2 givenname: Xingnan surname: Li fullname: Li, Xingnan organization: Department of Medicine, Division of Hematology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 3 givenname: Junjie surname: Zhu fullname: Zhu, Junjie organization: Department of Electrical Engineering, Stanford University School of Engineering, Stanford, CA, USA – sequence: 4 givenname: Valeria surname: Giangarra fullname: Giangarra, Valeria organization: 10x Genomics, Pleasanton, CA, USA – sequence: 5 givenname: Caitlin L. surname: Grzeskowiak fullname: Grzeskowiak, Caitlin L. organization: Department of Medicine, Division of Hematology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 6 givenname: Jihang surname: Ju fullname: Ju, Jihang organization: Department of Medicine, Division of Hematology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 7 givenname: Iris H. surname: Liu fullname: Liu, Iris H. organization: Department of Medicine, Division of Hematology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 8 givenname: Shin-Heng surname: Chiou fullname: Chiou, Shin-Heng organization: Institute for Immunity, Transplantation, and Infection, Stanford University School of Medicine, Stanford, CA, USA – sequence: 9 givenname: Ameen A. surname: Salahudeen fullname: Salahudeen, Ameen A. organization: Department of Medicine, Division of Hematology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 10 givenname: Amber R. surname: Smith fullname: Smith, Amber R. organization: Department of Medicine, Division of Hematology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 11 givenname: Brian C. surname: Deutsch fullname: Deutsch, Brian C. organization: Department of Medicine, Division of Hematology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 12 givenname: Lillian surname: Liao fullname: Liao, Lillian organization: Department of Medicine, Division of Hematology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 13 givenname: Allison J. surname: Zemek fullname: Zemek, Allison J. organization: Department of Pathology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 14 givenname: Fan surname: Zhao fullname: Zhao, Fan organization: Institute for Immunity, Transplantation, and Infection, Stanford University School of Medicine, Stanford, CA, USA – sequence: 15 givenname: Kasper surname: Karlsson fullname: Karlsson, Kasper organization: Department of Medicine, Division of Hematology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 16 givenname: Liora M. surname: Schultz fullname: Schultz, Liora M. organization: Department of Medicine, Division of Oncology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 17 givenname: Thomas J. surname: Metzner fullname: Metzner, Thomas J. organization: Department of Urology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 18 givenname: Lincoln D. surname: Nadauld fullname: Nadauld, Lincoln D. organization: Department of Medicine, Division of Hematology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 19 givenname: Yuen-Yi surname: Tseng fullname: Tseng, Yuen-Yi organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 20 givenname: Sahar surname: Alkhairy fullname: Alkhairy, Sahar organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 21 givenname: Coyin surname: Oh fullname: Oh, Coyin organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 22 givenname: Paula surname: Keskula fullname: Keskula, Paula organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 23 givenname: Daniel surname: Mendoza-Villanueva fullname: Mendoza-Villanueva, Daniel organization: TOMA Biosciences, Foster City, CA, USA – sequence: 24 givenname: Francisco M. surname: De La Vega fullname: De La Vega, Francisco M. organization: TOMA Biosciences, Foster City, CA, USA – sequence: 25 givenname: Pamela L. surname: Kunz fullname: Kunz, Pamela L. organization: Department of Medicine, Division of Oncology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 26 givenname: Joseph C. surname: Liao fullname: Liao, Joseph C. organization: Department of Urology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 27 givenname: John T. surname: Leppert fullname: Leppert, John T. organization: Department of Urology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 28 givenname: John B. surname: Sunwoo fullname: Sunwoo, John B. organization: Department of Otolaryngology, Stanford University School of Medicine, Stanford, CA, USA – sequence: 29 givenname: Chiara surname: Sabatti fullname: Sabatti, Chiara organization: Department of Biomedical Data Science, Stanford University School of Medicine, Stanford, CA, USA – sequence: 30 givenname: Jesse S. surname: Boehm fullname: Boehm, Jesse S. organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 31 givenname: William C. surname: Hahn fullname: Hahn, William C. organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 32 givenname: Grace X.Y. surname: Zheng fullname: Zheng, Grace X.Y. organization: 10x Genomics, Pleasanton, CA, USA – sequence: 33 givenname: Mark M. surname: Davis fullname: Davis, Mark M. organization: Institute for Immunity, Transplantation, and Infection, Stanford University School of Medicine, Stanford, CA, USA – sequence: 34 givenname: Calvin J. surname: Kuo fullname: Kuo, Calvin J. email: cjkuo@stanford.edu organization: Department of Medicine, Division of Hematology, Stanford University School of Medicine, Stanford, CA, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30550791$$D View this record in MEDLINE/PubMed |
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| Keywords | TCR T cell receptor immunotherapy tumor-infiltrating lymphocyte single-cell RNA-seq PDO cancer PD-1 checkpoint inhibitor organoid |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS J.T.N., X. L. and C.L.G. conceived, designed, and performed experiments, analyzed data, and wrote the manuscript. J.Z., G.X.Y.Z. and C.S. designed and analyzed single-cell studies. I.H.L, A.R.S., B.C.D, L.L., J.J., L.M.S. and L.D.N. designed and performed organoid experiments and analyzed data. V.G. and A.A.S. designed and performed single cell RNA-seq. K.K., Y-Y.T., S.A., C.O., P.K., D.M-V., F.M.DLV., J.S.B. and W.C.H participated in exome sequencing. A.J.Z. provided pathologic interpretation. J.B.S. designed patient-derived organoid studies. P.L.K, J.C.L., T.J.M and J.T.L. provided tumor samples. S-H.C., F.Z. and M.M.D. conceived and performed Smart-seq2 TCR sequencing and tetramer TIL detection. C.J.K. conceived and designed experiments, analyzed data and wrote the manuscript. |
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| SubjectTerms | Animals B7-H1 Antigen - immunology biopsy cancer checkpoint inhibitor coculture Coculture Techniques cytotoxicity epithelium Female hosts Humans Immunotherapy liquid-air interface macrophages Male Mice Mice, Inbred BALB C Models, Immunological Neoplasm Proteins - immunology neoplasms Neoplasms, Experimental - immunology Neoplasms, Experimental - pathology Neoplasms, Experimental - therapy organoid Organoids - immunology Organoids - pathology PD-1 PDO receptors Receptors, Antigen, T-Cell - immunology single-cell RNA-seq T cell receptor T-lymphocytes TCR Tumor Microenvironment - immunology tumor-infiltrating lymphocyte |
| Title | Organoid Modeling of the Tumor Immune Microenvironment |
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