Comparing neoantigen cancer vaccines and immune checkpoint therapy unveils an effective vaccine and anti-TREM2 macrophage-targeting dual therapy
The goal of therapeutic cancer vaccines and immune checkpoint therapy (ICT) is to promote T cells with anti-tumor capabilities. Here, we compared mutant neoantigen (neoAg) peptide-based vaccines with ICT in preclinical models. NeoAg vaccines induce the most robust expansion of proliferating and stem...
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| Published in: | Cell reports (Cambridge) Vol. 43; no. 11; p. 114875 |
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| Main Authors: | , , , , , , , , , , , , , , , , |
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26-11-2024
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| Abstract | The goal of therapeutic cancer vaccines and immune checkpoint therapy (ICT) is to promote T cells with anti-tumor capabilities. Here, we compared mutant neoantigen (neoAg) peptide-based vaccines with ICT in preclinical models. NeoAg vaccines induce the most robust expansion of proliferating and stem-like PD-1+TCF-1+ neoAg-specific CD8 T cells in tumors. Anti-CTLA-4 and/or anti-PD-1 ICT promotes intratumoral TCF-1− neoAg-specific CD8 T cells, although their phenotype depends in part on the specific ICT used. Anti-CTLA-4 also prompts substantial changes to CD4 T cells, including induction of ICOS+Bhlhe40+ T helper 1 (Th1)-like cells. Although neoAg vaccines or ICTs expand iNOS+ macrophages, neoAg vaccines maintain CX3CR1+CD206+ macrophages expressing the TREM2 receptor, unlike ICT, which suppresses them. TREM2 blockade enhances neoAg vaccine efficacy and is associated with fewer CX3CR1+CD206+ macrophages and induction of neoAg-specific CD8 T cells. Our findings highlight different mechanisms underlying neoAg vaccines and different forms of ICT and identify combinatorial therapies to enhance neoAg vaccine efficacy.
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•NeoAg vaccines utilize mechanisms partially distinct from those of αCTLA-4 or αPD-1•NeoAg vaccines potently induce TCF-1+ stem-like and proliferating neoAg-specific CD8 T cells•NeoAg vaccines induce macrophage remodeling partially distinct from that of αCTLA-4 or αPD-1•TREM2 blockade remodels intratumoral macrophages and enhances neoAg vaccine efficacy
Keshari et al. demonstrate in preclinical models that neoantigen peptide-based vaccines, anti-PD-1, and anti-CTLA-4 each induce partially distinct tumor microenvironment remodeling. Targeting intratumoral macrophages via TREM2 blockade extends the therapeutic window of neoantigen vaccines and is associated with a decrease in CX3CR1+CD206+ macrophages and the promotion of neoantigen-specific T cells. |
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| AbstractList | The goal of therapeutic cancer vaccines and immune checkpoint therapy (ICT) is to promote T cells with anti-tumor capabilities. Here, we compared mutant neoantigen (neoAg) peptide-based vaccines with ICT in preclinical models. NeoAg vaccines induce the most robust expansion of proliferating and stem-like PD-1+TCF-1+ neoAg-specific CD8 T cells in tumors. Anti-CTLA-4 and/or anti-PD-1 ICT promotes intratumoral TCF-1− neoAg-specific CD8 T cells, although their phenotype depends in part on the specific ICT used. Anti-CTLA-4 also prompts substantial changes to CD4 T cells, including induction of ICOS+Bhlhe40+ T helper 1 (Th1)-like cells. Although neoAg vaccines or ICTs expand iNOS+ macrophages, neoAg vaccines maintain CX3CR1+CD206+ macrophages expressing the TREM2 receptor, unlike ICT, which suppresses them. TREM2 blockade enhances neoAg vaccine efficacy and is associated with fewer CX3CR1+CD206+ macrophages and induction of neoAg-specific CD8 T cells. Our findings highlight different mechanisms underlying neoAg vaccines and different forms of ICT and identify combinatorial therapies to enhance neoAg vaccine efficacy.
[Display omitted]
•NeoAg vaccines utilize mechanisms partially distinct from those of αCTLA-4 or αPD-1•NeoAg vaccines potently induce TCF-1+ stem-like and proliferating neoAg-specific CD8 T cells•NeoAg vaccines induce macrophage remodeling partially distinct from that of αCTLA-4 or αPD-1•TREM2 blockade remodels intratumoral macrophages and enhances neoAg vaccine efficacy
Keshari et al. demonstrate in preclinical models that neoantigen peptide-based vaccines, anti-PD-1, and anti-CTLA-4 each induce partially distinct tumor microenvironment remodeling. Targeting intratumoral macrophages via TREM2 blockade extends the therapeutic window of neoantigen vaccines and is associated with a decrease in CX3CR1+CD206+ macrophages and the promotion of neoantigen-specific T cells. The goal of therapeutic cancer vaccines and immune checkpoint therapy (ICT) is to promote T cells with anti-tumor capabilities. Here, we compared mutant neoantigen (neoAg) peptide-based vaccines with ICT in preclinical models. NeoAg vaccines induce the most robust expansion of proliferating and stem-like PD-1+TCF-1+ neoAg-specific CD8 T cells in tumors. Anti-CTLA-4 and/or anti-PD-1 ICT promotes intratumoral TCF-1− neoAg-specific CD8 T cells, although their phenotype depends in part on the specific ICT used. Anti-CTLA-4 also prompts substantial changes to CD4 T cells, including induction of ICOS+Bhlhe40+ T helper 1 (Th1)-like cells. Although neoAg vaccines or ICTs expand iNOS+ macrophages, neoAg vaccines maintain CX3CR1+CD206+ macrophages expressing the TREM2 receptor, unlike ICT, which suppresses them. TREM2 blockade enhances neoAg vaccine efficacy and is associated with fewer CX3CR1+CD206+ macrophages and induction of neoAg-specific CD8 T cells. Our findings highlight different mechanisms underlying neoAg vaccines and different forms of ICT and identify combinatorial therapies to enhance neoAg vaccine efficacy. The goal of therapeutic cancer vaccines and immune checkpoint therapy (ICT) is to promote T cells with anti-tumor capabilities. Here, we compared mutant neoantigen (neoAg) peptide-based vaccines with ICT in preclinical models. NeoAg vaccines induce the most robust expansion of proliferating and stem-like PD-1+TCF-1+ neoAg-specific CD8 T cells in tumors. Anti-CTLA-4 and/or anti-PD-1 ICT promotes intratumoral TCF-1- neoAg-specific CD8 T cells, although their phenotype depends in part on the specific ICT used. Anti-CTLA-4 also prompts substantial changes to CD4 T cells, including induction of ICOS+Bhlhe40+ T helper 1 (Th1)-like cells. Although neoAg vaccines or ICTs expand iNOS+ macrophages, neoAg vaccines maintain CX3CR1+CD206+ macrophages expressing the TREM2 receptor, unlike ICT, which suppresses them. TREM2 blockade enhances neoAg vaccine efficacy and is associated with fewer CX3CR1+CD206+ macrophages and induction of neoAg-specific CD8 T cells. Our findings highlight different mechanisms underlying neoAg vaccines and different forms of ICT and identify combinatorial therapies to enhance neoAg vaccine efficacy.The goal of therapeutic cancer vaccines and immune checkpoint therapy (ICT) is to promote T cells with anti-tumor capabilities. Here, we compared mutant neoantigen (neoAg) peptide-based vaccines with ICT in preclinical models. NeoAg vaccines induce the most robust expansion of proliferating and stem-like PD-1+TCF-1+ neoAg-specific CD8 T cells in tumors. Anti-CTLA-4 and/or anti-PD-1 ICT promotes intratumoral TCF-1- neoAg-specific CD8 T cells, although their phenotype depends in part on the specific ICT used. Anti-CTLA-4 also prompts substantial changes to CD4 T cells, including induction of ICOS+Bhlhe40+ T helper 1 (Th1)-like cells. Although neoAg vaccines or ICTs expand iNOS+ macrophages, neoAg vaccines maintain CX3CR1+CD206+ macrophages expressing the TREM2 receptor, unlike ICT, which suppresses them. TREM2 blockade enhances neoAg vaccine efficacy and is associated with fewer CX3CR1+CD206+ macrophages and induction of neoAg-specific CD8 T cells. Our findings highlight different mechanisms underlying neoAg vaccines and different forms of ICT and identify combinatorial therapies to enhance neoAg vaccine efficacy. The goal of therapeutic cancer vaccines and immune checkpoint therapy (ICT) is to promote T cells with anti-tumor capabilities. Here, we compared mutant neoantigen (neoAg) peptide-based vaccines with ICT in preclinical models. NeoAg vaccines induce the most robust expansion of proliferating and stem-like PD-1 TCF-1 neoAg-specific CD8 T cells in tumors. Anti-CTLA-4 and/or anti-PD-1 ICT promotes intratumoral TCF-1 neoAg-specific CD8 T cells, although their phenotype depends in part on the specific ICT used. Anti-CTLA-4 also prompts substantial changes to CD4 T cells, including induction of ICOS Bhlhe40 T helper 1 (Th1)-like cells. Although neoAg vaccines or ICTs expand iNOS macrophages, neoAg vaccines maintain CX3CR1 CD206 macrophages expressing the TREM2 receptor, unlike ICT, which suppresses them. TREM2 blockade enhances neoAg vaccine efficacy and is associated with fewer CX3CR1 CD206 macrophages and induction of neoAg-specific CD8 T cells. Our findings highlight different mechanisms underlying neoAg vaccines and different forms of ICT and identify combinatorial therapies to enhance neoAg vaccine efficacy. |
| ArticleNumber | 114875 |
| Author | Alspach, Elise Saha, Akata Pineda, Josué E. Hu, Kenneth H. Miao, Qi Shavkunov, Alexander S. Gubin, Matthew M. Colonna, Marco Chaib, Mehdi Alekseev, Sayan Keshari, Sunita Molgora, Martina Pauken, Kristen E. Chen, Ken Minowa, Tomoyuki Williams, Charmelle D. Highsmith, Anna M. |
| Author_xml | – sequence: 1 givenname: Sunita surname: Keshari fullname: Keshari, Sunita organization: Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 2 givenname: Alexander S. surname: Shavkunov fullname: Shavkunov, Alexander S. organization: Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 3 givenname: Qi surname: Miao fullname: Miao, Qi organization: Department of Bioinformatics and Computational Biology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 4 givenname: Akata surname: Saha fullname: Saha, Akata organization: Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 5 givenname: Tomoyuki surname: Minowa fullname: Minowa, Tomoyuki organization: Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 6 givenname: Martina surname: Molgora fullname: Molgora, Martina organization: Department of Pathology and Immunology, Washington University School of Medicine in Saint Louis, St. Louis, MO, USA – sequence: 7 givenname: Charmelle D. surname: Williams fullname: Williams, Charmelle D. organization: Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 8 givenname: Mehdi surname: Chaib fullname: Chaib, Mehdi organization: Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 9 givenname: Anna M. surname: Highsmith fullname: Highsmith, Anna M. organization: Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 10 givenname: Josué E. surname: Pineda fullname: Pineda, Josué E. organization: Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 11 givenname: Sayan surname: Alekseev fullname: Alekseev, Sayan organization: Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 12 givenname: Elise surname: Alspach fullname: Alspach, Elise organization: Department of Molecular Microbiology and Immunology, Saint Louis University School of Medicine, St. Louis, MO, USA – sequence: 13 givenname: Kenneth H. surname: Hu fullname: Hu, Kenneth H. organization: Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 14 givenname: Marco surname: Colonna fullname: Colonna, Marco organization: Department of Pathology and Immunology, Washington University School of Medicine in Saint Louis, St. Louis, MO, USA – sequence: 15 givenname: Kristen E. surname: Pauken fullname: Pauken, Kristen E. organization: Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 16 givenname: Ken surname: Chen fullname: Chen, Ken organization: Department of Bioinformatics and Computational Biology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 17 givenname: Matthew M. surname: Gubin fullname: Gubin, Matthew M. email: mgubin@mdanderson.org organization: Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA |
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| Keywords | CP: Immunology neoantigen-specific CD8 T cells immune checkpoint therapy CP: Cancer cancer immunotherapy intratumoral macrophages combination immunotherapy neoantigen cancer vaccines anti-CTLA-4/anti-PD-1 CD4 T cells TREM2 tumor microenvironment |
| Language | English |
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| Snippet | The goal of therapeutic cancer vaccines and immune checkpoint therapy (ICT) is to promote T cells with anti-tumor capabilities. Here, we compared mutant... The goal of therapeutic cancer vaccines and immune checkpoint therapy (ICT) is to promote T cells with anti-tumor capabilities. Here, we compared mutant... |
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| SubjectTerms | anti-CTLA-4/anti-PD-1 cancer immunotherapy CD4 T cells combination immunotherapy CP: Cancer CP: Immunology immune checkpoint therapy intratumoral macrophages neoantigen cancer vaccines neoantigen-specific CD8 T cells TREM2 tumor microenvironment |
| Title | Comparing neoantigen cancer vaccines and immune checkpoint therapy unveils an effective vaccine and anti-TREM2 macrophage-targeting dual therapy |
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