Cancer cell plasticity defines response to immunotherapy in cutaneous squamous cell carcinoma

Immune checkpoint blockade (ICB) approaches have changed the therapeutic landscape for many tumor types. However, half of cutaneous squamous cell carcinoma (cSCC) patients remain unresponsive or develop resistance. Here, we show that, during cSCC progression in male mice, cancer cells acquire epithe...

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Published inNature communications Vol. 15; no. 1; pp. 5352 - 18
Main Authors Lorenzo-Sanz, Laura, Lopez-Cerda, Marta, da Silva-Diz, Victoria, Artés, Marta H, Llop, Sandra, Penin, Rosa M, Bermejo, Josep Oriol, Gonzalez-Suarez, Eva, Esteller, Manel, Viñals, Francesc, Espinosa, Enrique, Oliva, Marc, Piulats, Josep M, Martin-Liberal, Juan, Muñoz, Purificación
Format Journal Article
LanguageEnglish
Published England Nature Publishing Group 24.06.2024
Nature Portfolio
Subjects
Animals
Antitumor activity
B7-1 Antigen - metabolism
B7-H1 Antigen - antagonists & inhibitors
B7-H1 Antigen - metabolism
Blocking
Cancer
Carcinoma, Squamous Cell - drug therapy
Carcinoma, Squamous Cell - immunology
Carcinoma, Squamous Cell - pathology
Carcinoma, Squamous Cell - therapy
CD80 antigen
Cell Line, Tumor
Cell Plasticity - drug effects
CTLA-4 Antigen - antagonists & inhibitors
CTLA-4 Antigen - immunology
CTLA-4 Antigen - metabolism
CTLA-4 protein
E-cadherin
Epithelial-Mesenchymal Transition - immunology
Head and neck carcinoma
Humans
Immune checkpoint inhibitors
Immune Checkpoint Inhibitors - pharmacology
Immune Checkpoint Inhibitors - therapeutic use
Immune response
Immunosurveillance
Immunotherapy
Immunotherapy - methods
Ligands
Male
Melanoma
Mice
PD-1 protein
PD-L1 protein
Plastic properties
Plasticity
Programmed Cell Death 1 Receptor - antagonists & inhibitors
Programmed Cell Death 1 Receptor - metabolism
Receptors, Immunologic - metabolism
Receptors, Virus - genetics
Receptors, Virus - metabolism
Skin Neoplasms - drug therapy
Skin Neoplasms - immunology
Skin Neoplasms - pathology
Skin Neoplasms - therapy
Squamous cell carcinoma
Vimentin
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Abstract Immune checkpoint blockade (ICB) approaches have changed the therapeutic landscape for many tumor types. However, half of cutaneous squamous cell carcinoma (cSCC) patients remain unresponsive or develop resistance. Here, we show that, during cSCC progression in male mice, cancer cells acquire epithelial/mesenchymal plasticity and change their immune checkpoint (IC) ligand profile according to their features, dictating the IC pathways involved in immune evasion. Epithelial cancer cells, through the PD-1/PD-L1 pathway, and mesenchymal cancer cells, through the CTLA-4/CD80 and TIGIT/CD155 pathways, differentially block antitumor immune responses and determine the response to ICB therapies. Accordingly, the anti-PD-L1/TIGIT combination is the most effective strategy for blocking the growth of cSCCs that contain both epithelial and mesenchymal cancer cells. The expression of E-cadherin/Vimentin/CD80/CD155 proteins in cSCC, HNSCC and melanoma patient samples predicts response to anti-PD-1/PD-L1 therapy. Collectively, our findings indicate that the selection of ICB therapies should take into account the epithelial/mesenchymal features of cancer cells.
AbstractList Abstract Immune checkpoint blockade (ICB) approaches have changed the therapeutic landscape for many tumor types. However, half of cutaneous squamous cell carcinoma (cSCC) patients remain unresponsive or develop resistance. Here, we show that, during cSCC progression in male mice, cancer cells acquire epithelial/mesenchymal plasticity and change their immune checkpoint (IC) ligand profile according to their features, dictating the IC pathways involved in immune evasion. Epithelial cancer cells, through the PD-1/PD-L1 pathway, and mesenchymal cancer cells, through the CTLA-4/CD80 and TIGIT/CD155 pathways, differentially block antitumor immune responses and determine the response to ICB therapies. Accordingly, the anti-PD-L1/TIGIT combination is the most effective strategy for blocking the growth of cSCCs that contain both epithelial and mesenchymal cancer cells. The expression of E-cadherin/Vimentin/CD80/CD155 proteins in cSCC, HNSCC and melanoma patient samples predicts response to anti-PD-1/PD-L1 therapy. Collectively, our findings indicate that the selection of ICB therapies should take into account the epithelial/mesenchymal features of cancer cells.
Immune checkpoint blockade (ICB) approaches have changed the therapeutic landscape for many tumor types. However, half of cutaneous squamous cell carcinoma (cSCC) patients remain unresponsive or develop resistance. Here, we show that, during cSCC progression in male mice, cancer cells acquire epithelial/mesenchymal plasticity and change their immune checkpoint (IC) ligand profile according to their features, dictating the IC pathways involved in immune evasion. Epithelial cancer cells, through the PD-1/PD-L1 pathway, and mesenchymal cancer cells, through the CTLA-4/CD80 and TIGIT/CD155 pathways, differentially block antitumor immune responses and determine the response to ICB therapies. Accordingly, the anti-PD-L1/TIGIT combination is the most effective strategy for blocking the growth of cSCCs that contain both epithelial and mesenchymal cancer cells. The expression of E-cadherin/Vimentin/CD80/CD155 proteins in cSCC, HNSCC and melanoma patient samples predicts response to anti-PD-1/PD-L1 therapy. Collectively, our findings indicate that the selection of ICB therapies should take into account the epithelial/mesenchymal features of cancer cells.
Immune checkpoint blockade (ICB) approaches have changed the therapeutic landscape for many tumor types. However, half of cutaneous squamous cell carcinoma (cSCC) patients remain unresponsive or develop resistance. Here, we show that, during cSCC progression in male mice, cancer cells acquire epithelial/mesenchymal plasticity and change their immune checkpoint (IC) ligand profile according to their features, dictating the IC pathways involved in immune evasion. Epithelial cancer cells, through the PD-1/PD-L1 pathway, and mesenchymal cancer cells, through the CTLA-4/CD80 and TIGIT/CD155 pathways, differentially block antitumor immune responses and determine the response to ICB therapies. Accordingly, the anti-PD-L1/TIGIT combination is the most effective strategy for blocking the growth of cSCCs that contain both epithelial and mesenchymal cancer cells. The expression of E-cadherin/Vimentin/CD80/CD155 proteins in cSCC, HNSCC and melanoma patient samples predicts response to anti-PD-1/PD-L1 therapy. Collectively, our findings indicate that the selection of ICB therapies should take into account the epithelial/mesenchymal features of cancer cells.Immune surveillance is critical to prevent the development and progression of cutaneous squamous cell carcinoma (cSCC). Here, the authors show that epithelial-mesenchymal plasticity in cancer cells is associated with changes in their immune checkpoint ligand profile during mouse cSCC progression, which dictates differential responses to immune checkpoint blockade.
Immune checkpoint blockade (ICB) approaches have changed the therapeutic landscape for many tumor types. However, half of cutaneous squamous cell carcinoma (cSCC) patients remain unresponsive or develop resistance. Here, we show that, during cSCC progression in male mice, cancer cells acquire epithelial/mesenchymal plasticity and change their immune checkpoint (IC) ligand profile according to their features, dictating the IC pathways involved in immune evasion. Epithelial cancer cells, through the PD-1/PD-L1 pathway, and mesenchymal cancer cells, through the CTLA-4/CD80 and TIGIT/CD155 pathways, differentially block antitumor immune responses and determine the response to ICB therapies. Accordingly, the anti-PD-L1/TIGIT combination is the most effective strategy for blocking the growth of cSCCs that contain both epithelial and mesenchymal cancer cells. The expression of E-cadherin/Vimentin/CD80/CD155 proteins in cSCC, HNSCC and melanoma patient samples predicts response to anti-PD-1/PD-L1 therapy. Collectively, our findings indicate that the selection of ICB therapies should take into account the epithelial/mesenchymal features of cancer cells.Immune checkpoint blockade (ICB) approaches have changed the therapeutic landscape for many tumor types. However, half of cutaneous squamous cell carcinoma (cSCC) patients remain unresponsive or develop resistance. Here, we show that, during cSCC progression in male mice, cancer cells acquire epithelial/mesenchymal plasticity and change their immune checkpoint (IC) ligand profile according to their features, dictating the IC pathways involved in immune evasion. Epithelial cancer cells, through the PD-1/PD-L1 pathway, and mesenchymal cancer cells, through the CTLA-4/CD80 and TIGIT/CD155 pathways, differentially block antitumor immune responses and determine the response to ICB therapies. Accordingly, the anti-PD-L1/TIGIT combination is the most effective strategy for blocking the growth of cSCCs that contain both epithelial and mesenchymal cancer cells. The expression of E-cadherin/Vimentin/CD80/CD155 proteins in cSCC, HNSCC and melanoma patient samples predicts response to anti-PD-1/PD-L1 therapy. Collectively, our findings indicate that the selection of ICB therapies should take into account the epithelial/mesenchymal features of cancer cells.
ArticleNumber 5352
Author Llop, Sandra
Martin-Liberal, Juan
Penin, Rosa M
Artés, Marta H
Lorenzo-Sanz, Laura
Piulats, Josep M
Gonzalez-Suarez, Eva
Muñoz, Purificación
da Silva-Diz, Victoria
Bermejo, Josep Oriol
Esteller, Manel
Viñals, Francesc
Lopez-Cerda, Marta
Oliva, Marc
Espinosa, Enrique
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Snippet Immune checkpoint blockade (ICB) approaches have changed the therapeutic landscape for many tumor types. However, half of cutaneous squamous cell carcinoma...
Abstract Immune checkpoint blockade (ICB) approaches have changed the therapeutic landscape for many tumor types. However, half of cutaneous squamous cell...
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SubjectTerms Animals
Antitumor activity
B7-1 Antigen - metabolism
B7-H1 Antigen - antagonists & inhibitors
B7-H1 Antigen - metabolism
Blocking
Cancer
Carcinoma, Squamous Cell - drug therapy
Carcinoma, Squamous Cell - immunology
Carcinoma, Squamous Cell - pathology
Carcinoma, Squamous Cell - therapy
CD80 antigen
Cell Line, Tumor
Cell Plasticity - drug effects
CTLA-4 Antigen - antagonists & inhibitors
CTLA-4 Antigen - immunology
CTLA-4 Antigen - metabolism
CTLA-4 protein
E-cadherin
Epithelial-Mesenchymal Transition - immunology
Head and neck carcinoma
Humans
Immune checkpoint inhibitors
Immune Checkpoint Inhibitors - pharmacology
Immune Checkpoint Inhibitors - therapeutic use
Immune response
Immunosurveillance
Immunotherapy
Immunotherapy - methods
Ligands
Male
Melanoma
Mice
PD-1 protein
PD-L1 protein
Plastic properties
Plasticity
Programmed Cell Death 1 Receptor - antagonists & inhibitors
Programmed Cell Death 1 Receptor - metabolism
Receptors, Immunologic - metabolism
Receptors, Virus - genetics
Receptors, Virus - metabolism
Skin Neoplasms - drug therapy
Skin Neoplasms - immunology
Skin Neoplasms - pathology
Skin Neoplasms - therapy
Squamous cell carcinoma
Vimentin
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Title Cancer cell plasticity defines response to immunotherapy in cutaneous squamous cell carcinoma
URI https://www.ncbi.nlm.nih.gov/pubmed/38914547
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