Identification of CMTM6 and CMTM4 as PD-L1 protein regulators
CMTM6 and CMTM4 bind to and stabilize the inhibitory receptor PD-L1 and regulate PD-L1 levels at the surface of human tumour and immune cells. Regulating immunity evasion PD-1/PD-L1 blocking antibodies are effective in the treatment of various cancers. In this study, Ton Schumacher and colleagues de...
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| Vydané v: | Nature (London) Ročník 549; číslo 7670; s. 106 - 110 |
|---|---|
| Hlavní autori: | , , , , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
| Vydavateľské údaje: |
London
Nature Publishing Group UK
07.09.2017
Nature Publishing Group |
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| ISSN: | 0028-0836, 1476-4687, 1476-4687 |
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| Abstract | CMTM6 and CMTM4 bind to and stabilize the inhibitory receptor PD-L1 and regulate PD-L1 levels at the surface of human tumour and immune cells.
Regulating immunity evasion
PD-1/PD-L1 blocking antibodies are effective in the treatment of various cancers. In this study, Ton Schumacher and colleagues describe a haploid genetic screen to identify molecules and pathways that influence the cell surface expression of PD-L1. They identify chemokine-like factors CMTM6 and CMTM4 as cell endogenous regulators of PD-L1 stability, and suggest that this axis could be targeted therapeutically to improve cancer immunotherapy. Elsewhere in this issue, Mark Dawson and colleagues also identify CMTM6 as a novel regulator of PD-L1 expression, through a genome-wide CRISPR–Cas9 screen. CMTM6 functions to maintain PD-L1 at the plasma membrane by inhibiting its lysosome-mediated degradation and promoting its recycling.
The clinical benefit for patients with diverse types of metastatic cancers that has been observed upon blockade of the interaction between PD-1 and PD-L1 has highlighted the importance of this inhibitory axis in the suppression of tumour-specific T-cell responses
1
,
2
,
3
,
4
,
5
,
6
,
7
,
8
,
9
. Notwithstanding the key role of PD-L1 expression by cells within the tumour micro-environment, our understanding of the regulation of the PD-L1 protein is limited
10
,
11
,
12
,
13
,
14
,
15
. Here we identify, using a haploid genetic screen, CMTM6, a type-3 transmembrane protein of previously unknown function, as a regulator of the PD-L1 protein. Interference with CMTM6 expression results in impaired PD-L1 protein expression in all human tumour cell types tested and in primary human dendritic cells. Furthermore, through both a haploid genetic modifier screen in CMTM6-deficient cells and genetic complementation experiments, we demonstrate that this function is shared by its closest family member, CMTM4, but not by any of the other CMTM members tested. Notably, CMTM6 increases the PD-L1 protein pool without affecting
PD-L1
(also known as
CD274
) transcription levels. Rather, we demonstrate that CMTM6 is present at the cell surface, associates with the PD-L1 protein, reduces its ubiquitination and increases PD-L1 protein half-life. Consistent with its role in PD-L1 protein regulation, CMTM6 enhances the ability of PD-L1-expressing tumour cells to inhibit T cells. Collectively, our data reveal that PD-L1 relies on CMTM6/4 to efficiently carry out its inhibitory function, and suggest potential new avenues to block this pathway. |
|---|---|
| AbstractList | The clinical benefit for patients with diverse types of metastatic cancers that has been observed upon blockade of the interaction between PD-1 and PD-L1 has highlighted the importance of this inhibitory axis in the suppression of tumour-specific T-cell responses. Notwithstanding the key role of PD-L1 expression by cells within the tumour micro-environment, our understanding of the regulation of the PD-L1 protein is limited. Here we identify, using a haploid genetic screen, CMTM6, a type-3 transmembrane protein of previously unknown function, as a regulator of the PD-L1 protein. Interference with CMTM6 expression results in impaired PD-L1 protein expression in all human tumour cell types tested and in primary human dendritic cells. Furthermore, through both a haploid genetic modifier screen in CMTM6-deficient cells and genetic complementation experiments, we demonstrate that this function is shared by its closest family member, CMTM4, but not by any of the other CMTM members tested. Notably, CMTM6 increases the PD-L1 protein pool without affecting PD-L1 (also known as CD274) transcription levels. Rather, we demonstrate that CMTM6 is present at the cell surface, associates with the PD-L1 protein, reduces its ubiquitination and increases PD-L1 protein half-life. Consistent with its role in PD-L1 protein regulation, CMTM6 enhances the ability of PD-L1-expressing tumour cells to inhibit T cells. Collectively, our data reveal that PD-L1 relies on CMTM6/4 to efficiently carry out its inhibitory function, and suggest potential new avenues to block this pathway. The clinical benefit for patients with diverse types of metastatic cancers that has been observed upon blockade of the interaction between PD-1 and PD-L1 has highlighted the importance of this inhibitory axis in the suppression of tumour-specific T-cell responses. Notwithstanding the key role of PD-L1 expression by cells within the tumour micro-environment, our understanding of the regulation of the PD-L1 protein is limited. Here we identify, using a haploid genetic screen, CMTM6, a type-3 transmembrane protein of previously unknown function, as a regulator of the PD-L1 protein. Interference with CMTM6 expression results in impaired PD-L1 protein expression in all human tumour cell types tested and in primary human dendritic cells. Furthermore, through both a haploid genetic modifier screen in CMTM6-deficient cells and genetic complementation experiments, we demonstrate that this function is shared by its closest family member, CMTM4, but not by any of the other CMTM members tested. Notably, CMTM6 increases the PD-L1 protein pool without affecting PD-L1 (also known as CD274) transcription levels. Rather, we demonstrate that CMTM6 is present at the cell surface, associates with the PD-L1 protein, reduces its ubiquitination and increases PD-L1 protein half-life. Consistent with its role in PD-L1 protein regulation, CMTM6 enhances the ability of PD-L1-expressing tumour cells to inhibit T cells. Collectively, our data reveal that PD-L1 relies on CMTM6/4 to efficiently carry out its inhibitory function, and suggest potential new avenues to block this pathway.The clinical benefit for patients with diverse types of metastatic cancers that has been observed upon blockade of the interaction between PD-1 and PD-L1 has highlighted the importance of this inhibitory axis in the suppression of tumour-specific T-cell responses. Notwithstanding the key role of PD-L1 expression by cells within the tumour micro-environment, our understanding of the regulation of the PD-L1 protein is limited. Here we identify, using a haploid genetic screen, CMTM6, a type-3 transmembrane protein of previously unknown function, as a regulator of the PD-L1 protein. Interference with CMTM6 expression results in impaired PD-L1 protein expression in all human tumour cell types tested and in primary human dendritic cells. Furthermore, through both a haploid genetic modifier screen in CMTM6-deficient cells and genetic complementation experiments, we demonstrate that this function is shared by its closest family member, CMTM4, but not by any of the other CMTM members tested. Notably, CMTM6 increases the PD-L1 protein pool without affecting PD-L1 (also known as CD274) transcription levels. Rather, we demonstrate that CMTM6 is present at the cell surface, associates with the PD-L1 protein, reduces its ubiquitination and increases PD-L1 protein half-life. Consistent with its role in PD-L1 protein regulation, CMTM6 enhances the ability of PD-L1-expressing tumour cells to inhibit T cells. Collectively, our data reveal that PD-L1 relies on CMTM6/4 to efficiently carry out its inhibitory function, and suggest potential new avenues to block this pathway. The clinical benefit in patients with diverse types of metastatic cancers that is observed upon blockade of the PD-1 – PD-L1 interaction has highlighted the importance of this inhibitory axis in the suppression of tumor-specific T cell responses1–9. In spite of the key role of PD-L1 expression by cells within the tumor micro-environment, our understanding of the regulation of the PD-L1 protein is limited10–15. Using a haploid genetic screen, we here identify CMTM6, a type 3 transmembrane protein of previously unknown function, as a regulator of the PD-L1 protein. Interference with CMTM6 expression results in impaired PD-L1 protein expression in all tumor cell types tested and in primary human dendritic cells. Furthermore, through both a haploid genetic modifier screen in CMTM6 deficient cells and genetic complementation experiments, we demonstrate that this function is shared by its closest family member CMTM4, but not by all other CMTM members tested. Notably, CMTM6 increases the PD-L1 protein pool without affecting PD-L1 transcript levels. Rather, we demonstrate that CMTM6 is present at the cell surface, associates with the PD-L1 protein, reduces its ubiquitination and increases PD-L1 protein half-life. Consistent with its role in PD-L1 protein regulation, T cell inhibitory capacity of PD-L1 expressing tumor cells is enhanced by CMTM6. Collectively, our data reveal that PD-L1 relies on CMTM6/4 to efficiently carry out its inhibitory function, and suggest potential new avenues to block this pathway. CMTM6 and CMTM4 bind to and stabilize the inhibitory receptor PD-L1 and regulate PD-L1 levels at the surface of human tumour and immune cells. Regulating immunity evasion PD-1/PD-L1 blocking antibodies are effective in the treatment of various cancers. In this study, Ton Schumacher and colleagues describe a haploid genetic screen to identify molecules and pathways that influence the cell surface expression of PD-L1. They identify chemokine-like factors CMTM6 and CMTM4 as cell endogenous regulators of PD-L1 stability, and suggest that this axis could be targeted therapeutically to improve cancer immunotherapy. Elsewhere in this issue, Mark Dawson and colleagues also identify CMTM6 as a novel regulator of PD-L1 expression, through a genome-wide CRISPR–Cas9 screen. CMTM6 functions to maintain PD-L1 at the plasma membrane by inhibiting its lysosome-mediated degradation and promoting its recycling. The clinical benefit for patients with diverse types of metastatic cancers that has been observed upon blockade of the interaction between PD-1 and PD-L1 has highlighted the importance of this inhibitory axis in the suppression of tumour-specific T-cell responses 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 . Notwithstanding the key role of PD-L1 expression by cells within the tumour micro-environment, our understanding of the regulation of the PD-L1 protein is limited 10 , 11 , 12 , 13 , 14 , 15 . Here we identify, using a haploid genetic screen, CMTM6, a type-3 transmembrane protein of previously unknown function, as a regulator of the PD-L1 protein. Interference with CMTM6 expression results in impaired PD-L1 protein expression in all human tumour cell types tested and in primary human dendritic cells. Furthermore, through both a haploid genetic modifier screen in CMTM6-deficient cells and genetic complementation experiments, we demonstrate that this function is shared by its closest family member, CMTM4, but not by any of the other CMTM members tested. Notably, CMTM6 increases the PD-L1 protein pool without affecting PD-L1 (also known as CD274 ) transcription levels. Rather, we demonstrate that CMTM6 is present at the cell surface, associates with the PD-L1 protein, reduces its ubiquitination and increases PD-L1 protein half-life. Consistent with its role in PD-L1 protein regulation, CMTM6 enhances the ability of PD-L1-expressing tumour cells to inhibit T cells. Collectively, our data reveal that PD-L1 relies on CMTM6/4 to efficiently carry out its inhibitory function, and suggest potential new avenues to block this pathway. |
| Audience | Academic |
| Author | Sun, Chong Gomez-Eerland, Raquel Rozeman, Elisa A. Slagter, Maarten Wu, Wei Horlings, Hugo M. Xiao, Yanling Hofland, Ingrid Wessels, Lodewyk F. A. Mezzadra, Riccardo Logtenberg, Meike E. W. Jae, Lucas T. de Vries, Evert Broeks, Annegien Schumacher, Ton N. M. Heck, Albert J. R. Brummelkamp, Thijn R. Blank, Christian U. Borst, Jannie |
| AuthorAffiliation | 5 Biomolecular Mass Spectrometry and Proteomics, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, Utrecht University, Utrecht, The Netherlands 2 Division of Biochemistry, The Netherlands Cancer Institute, Amsterdam, The Netherlands 9 Core Facility Molecular Pathology & Biobanking, Division of Pathology, The Netherlands Cancer Institute, Amsterdam, The Netherlands 7 Division of Molecular Carcinogenesis, The Netherlands Cancer Institute, Amsterdam, The Netherlands 12 CGC.nl 1 Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute, Amsterdam, The Netherlands 4 Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, The Netherlands 6 Netherlands Proteomics Centre, Utrecht, The Netherlands 8 Division of Medical Oncology, The Netherlands Cancer Institute, Amsterdam, The Netherlands 10 Division of Pathology, The Netherlands Cancer Institute, Amsterdam, The Netherlands 11 CeMM Research Center for Molecular Med |
| AuthorAffiliation_xml | – name: 1 Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute, Amsterdam, The Netherlands – name: 5 Biomolecular Mass Spectrometry and Proteomics, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, Utrecht University, Utrecht, The Netherlands – name: 8 Division of Medical Oncology, The Netherlands Cancer Institute, Amsterdam, The Netherlands – name: 6 Netherlands Proteomics Centre, Utrecht, The Netherlands – name: 7 Division of Molecular Carcinogenesis, The Netherlands Cancer Institute, Amsterdam, The Netherlands – name: 9 Core Facility Molecular Pathology & Biobanking, Division of Pathology, The Netherlands Cancer Institute, Amsterdam, The Netherlands – name: 10 Division of Pathology, The Netherlands Cancer Institute, Amsterdam, The Netherlands – name: 4 Division of Tumor Biology & Immunology, The Netherlands Cancer Institute, Amsterdam, The Netherlands – name: 11 CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, 1090 Vienna, Austria – name: 2 Division of Biochemistry, The Netherlands Cancer Institute, Amsterdam, The Netherlands – name: 12 CGC.nl |
| Author_xml | – sequence: 1 givenname: Riccardo surname: Mezzadra fullname: Mezzadra, Riccardo organization: Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute – sequence: 2 givenname: Chong surname: Sun fullname: Sun, Chong organization: Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute – sequence: 3 givenname: Lucas T. surname: Jae fullname: Jae, Lucas T. organization: Division of Biochemistry, The Netherlands Cancer Institute, Gene Center and Department of Biochemistry, Ludwig-Maximilians-Universität München – sequence: 4 givenname: Raquel surname: Gomez-Eerland fullname: Gomez-Eerland, Raquel organization: Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute – sequence: 5 givenname: Evert surname: de Vries fullname: de Vries, Evert organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute – sequence: 6 givenname: Wei surname: Wu fullname: Wu, Wei organization: Biomolecular Mass Spectrometry and Proteomics, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, Netherlands Proteomics Centre – sequence: 7 givenname: Meike E. W. surname: Logtenberg fullname: Logtenberg, Meike E. W. organization: Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute – sequence: 8 givenname: Maarten surname: Slagter fullname: Slagter, Maarten organization: Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute, Division of Molecular Carcinogenesis, The Netherlands Cancer Institute – sequence: 9 givenname: Elisa A. surname: Rozeman fullname: Rozeman, Elisa A. organization: Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute, Division of Medical Oncology, The Netherlands Cancer Institute – sequence: 10 givenname: Ingrid surname: Hofland fullname: Hofland, Ingrid organization: Division of Pathology, Core Facility Molecular Pathology & Biobanking, The Netherlands Cancer Institute – sequence: 11 givenname: Annegien surname: Broeks fullname: Broeks, Annegien organization: Division of Pathology, Core Facility Molecular Pathology & Biobanking, The Netherlands Cancer Institute – sequence: 12 givenname: Hugo M. surname: Horlings fullname: Horlings, Hugo M. organization: Division of Pathology, The Netherlands Cancer Institute – sequence: 13 givenname: Lodewyk F. A. surname: Wessels fullname: Wessels, Lodewyk F. A. organization: Division of Molecular Carcinogenesis, The Netherlands Cancer Institute – sequence: 14 givenname: Christian U. surname: Blank fullname: Blank, Christian U. organization: Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute, Division of Medical Oncology, The Netherlands Cancer Institute – sequence: 15 givenname: Yanling surname: Xiao fullname: Xiao, Yanling organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute – sequence: 16 givenname: Albert J. R. surname: Heck fullname: Heck, Albert J. R. organization: Biomolecular Mass Spectrometry and Proteomics, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, Netherlands Proteomics Centre – sequence: 17 givenname: Jannie surname: Borst fullname: Borst, Jannie organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute – sequence: 18 givenname: Thijn R. surname: Brummelkamp fullname: Brummelkamp, Thijn R. email: t.brummelkamp@nki.nl organization: Division of Biochemistry, The Netherlands Cancer Institute, CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Cancergenomics.nl – sequence: 19 givenname: Ton N. M. surname: Schumacher fullname: Schumacher, Ton N. M. email: t.schumacher@nki.nl organization: Division of Molecular Oncology & Immunology, The Netherlands Cancer Institute |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28813410$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Macmillan Publishers Limited, part of Springer Nature. All rights reserved. 2017 COPYRIGHT 2017 Nature Publishing Group Copyright Nature Publishing Group Sep 7, 2017 |
| Copyright_xml | – notice: Macmillan Publishers Limited, part of Springer Nature. All rights reserved. 2017 – notice: COPYRIGHT 2017 Nature Publishing Group – notice: Copyright Nature Publishing Group Sep 7, 2017 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Present address: Gene Center and Department of Biochemistry, Ludwig-Maximilians-Universität München, Feodor-Lynen-Str. 25, 81377 Munich, Germany |
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| Snippet | CMTM6 and CMTM4 bind to and stabilize the inhibitory receptor PD-L1 and regulate PD-L1 levels at the surface of human tumour and immune cells.
Regulating... The clinical benefit for patients with diverse types of metastatic cancers that has been observed upon blockade of the interaction between PD-1 and PD-L1 has... The clinical benefit in patients with diverse types of metastatic cancers that is observed upon blockade of the PD-1 – PD-L1 interaction has highlighted the... |
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| SubjectTerms | 13/1 13/106 13/109 13/21 13/31 13/44 13/51 13/89 38/47 38/70 38/77 38/89 631/208/200 631/250/251/1574 B7-H1 Antigen - biosynthesis B7-H1 Antigen - chemistry B7-H1 Antigen - metabolism Cancer cells Cancer metastasis Cell Line, Tumor Cell surface CRISPR-Cas Systems Dendritic cells Dendritic Cells - metabolism Genetic Complementation Test Genetic screening Haploidy Humanities and Social Sciences Humans L1 protein letter Lymphocytes Lymphocytes T MARVEL Domain-Containing Proteins - genetics MARVEL Domain-Containing Proteins - metabolism Mass spectrometry Medical research Melanoma Melanoma - genetics Melanoma - metabolism Metastases multidisciplinary PD-1 protein PD-L1 protein Physiological aspects Protein Binding Protein Stability Proteins Science Scientific imaging T cells Thyroid cancer Transcription Tumors Ubiquitination |
| Title | Identification of CMTM6 and CMTM4 as PD-L1 protein regulators |
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