Identification of Neoantigens in Two Murine Gastric Cancer Cell Lines Leading to the Neoantigen-Based Immunotherapy
To develop combination immunotherapies for gastric cancers, immunologically well-characterized preclinical models are crucial. Here, we leveraged two transplantable murine gastric cancer cell lines, YTN2 and YTN16, derived from the same parental line but differing in their susceptibility to immune r...
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Published in | Cancers Vol. 14; no. 1; p. 106 |
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Main Authors | , , , , , , , , , , , , |
Format | Journal Article |
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27.12.2021
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Abstract | To develop combination immunotherapies for gastric cancers, immunologically well-characterized preclinical models are crucial. Here, we leveraged two transplantable murine gastric cancer cell lines, YTN2 and YTN16, derived from the same parental line but differing in their susceptibility to immune rejection. We established their differential sensitivity to immune checkpoint inhibitors (ICI) and identified neoantigens. Although anti-CTLA-4 mAbs eradicated YTN16 tumors in 4 of 5 mice, anti-PD-1 and anti-PD-L1 mAbs failed to eradicate YTN16 tumors. Using whole-exome and RNA sequencing, we identified two and three neoantigens in YTN2 and YTN16, respectively. MHC class I ligandome analysis detected the expression of only one of these neoantigens, mutated Cdt1, but the exact length of MHC binding peptide was determined. Dendritic cell vaccine loaded with neoepitope peptides and adoptive transfer of neoantigen-specific CD8
T cells successfully inhibited the YTN16 tumor growth. Targeting mutated Cdt1 had better efficacy for controlling the tumor. Therefore, mutated Cdt1 was the dominant neoantigen in these tumor cells. More mCdt1 peptides were bound to MHC class I and presented on YTN2 surface than YTN16. This might be one of the reasons why YTN2 was rejected while YTN16 grew in immune-competent mice. |
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AbstractList | To develop combination immunotherapies for gastric cancers, immunologically well-characterized preclinical models are crucial. Here, we leveraged two transplantable murine gastric cancer cell lines, YTN2 and YTN16, derived from the same parental line but differing in their susceptibility to immune rejection. We established their differential sensitivity to immune checkpoint inhibitors (ICI) and identified neoantigens. Although anti-CTLA-4 mAbs eradicated YTN16 tumors in 4 of 5 mice, anti-PD-1 and anti-PD-L1 mAbs failed to eradicate YTN16 tumors. Using whole-exome and RNA sequencing, we identified two and three neoantigens in YTN2 and YTN16, respectively. MHC class I ligandome analysis detected the expression of only one of these neoantigens, mutated Cdt1, but the exact length of MHC binding peptide was determined. Dendritic cell vaccine loaded with neoepitope peptides and adoptive transfer of neoantigen-specific CD8
T cells successfully inhibited the YTN16 tumor growth. Targeting mutated Cdt1 had better efficacy for controlling the tumor. Therefore, mutated Cdt1 was the dominant neoantigen in these tumor cells. More mCdt1 peptides were bound to MHC class I and presented on YTN2 surface than YTN16. This might be one of the reasons why YTN2 was rejected while YTN16 grew in immune-competent mice. Simple SummaryDespite the success of immune checkpoint inhibitors (ICI) for treating a variety of solid cancers, most gastric cancer patients are resistant to ICI monotherapies. Combinations of ICI with other therapies may be able to overcome this resistance. In order to develop combination immunotherapies, immunologically well-characterized preclinical gastric cancer models are required. To this end, in the present study, we characterized two murine gastric cancer cell lines, namely, YTN2 which spontaneously regresses, and YTN16 which grows progressively. Although anti-CTLA-4 monotherapy eradicated most YTN16 tumors, these were resistant to either anti-PD-1 or anti-PD-L1 treatment. Furthermore, we identified neoantigens in YTN2 and YTN16 tumors and conducted neoantigen-based immunotherapy for these tumors. In addition, the information on neoantigens facilitates the evaluation of tumor-specific immune responses induced by the combination therapies. These immunologically well-characterized gastric cancer models will contribute to the development of novel combination immunotherapies.AbstractTo develop combination immunotherapies for gastric cancers, immunologically well-characterized preclinical models are crucial. Here, we leveraged two transplantable murine gastric cancer cell lines, YTN2 and YTN16, derived from the same parental line but differing in their susceptibility to immune rejection. We established their differential sensitivity to immune checkpoint inhibitors (ICI) and identified neoantigens. Although anti-CTLA-4 mAbs eradicated YTN16 tumors in 4 of 5 mice, anti-PD-1 and anti-PD-L1 mAbs failed to eradicate YTN16 tumors. Using whole-exome and RNA sequencing, we identified two and three neoantigens in YTN2 and YTN16, respectively. MHC class I ligandome analysis detected the expression of only one of these neoantigens, mutated Cdt1, but the exact length of MHC binding peptide was determined. Dendritic cell vaccine loaded with neoepitope peptides and adoptive transfer of neoantigen-specific CD8+ T cells successfully inhibited the YTN16 tumor growth. Targeting mutated Cdt1 had better efficacy for controlling the tumor. Therefore, mutated Cdt1 was the dominant neoantigen in these tumor cells. More mCdt1 peptides were bound to MHC class I and presented on YTN2 surface than YTN16. This might be one of the reasons why YTN2 was rejected while YTN16 grew in immune-competent mice. To develop combination immunotherapies for gastric cancers, immunologically well-characterized preclinical models are crucial. Here, we leveraged two transplantable murine gastric cancer cell lines, YTN2 and YTN16, derived from the same parental line but differing in their susceptibility to immune rejection. We established their differential sensitivity to immune checkpoint inhibitors (ICI) and identified neoantigens. Although anti-CTLA-4 mAbs eradicated YTN16 tumors in 4 of 5 mice, anti-PD-1 and anti-PD-L1 mAbs failed to eradicate YTN16 tumors. Using whole-exome and RNA sequencing, we identified two and three neoantigens in YTN2 and YTN16, respectively. MHC class I ligandome analysis detected the expression of only one of these neoantigens, mutated Cdt1, but the exact length of MHC binding peptide was determined. Dendritic cell vaccine loaded with neoepitope peptides and adoptive transfer of neoantigen-specific CD8+ T cells successfully inhibited the YTN16 tumor growth. Targeting mutated Cdt1 had better efficacy for controlling the tumor. Therefore, mutated Cdt1 was the dominant neoantigen in these tumor cells. More mCdt1 peptides were bound to MHC class I and presented on YTN2 surface than YTN16. This might be one of the reasons why YTN2 was rejected while YTN16 grew in immune-competent mice. |
Author | Kakimi, Kazuhiro Nomura, Sachiyo Nakagawa, Hidewaki Futami, Junichiro Kobayashi, Yukari Tokita, Serina Kanaseki, Takayuki Torigoe, Toshihiko Udaka, Keiko Maejima, Kazuhiro Nagaoka, Koji Komatsu, Toshihiro Sun, Changbo |
AuthorAffiliation | 3 Sapporo Dohto Hospital, Sapporo 065-0017, Japan 4 Department of Immunology, Kochi University, Kochi 783-8505, Japan; tkomatsu@kochi-u.ac.jp (T.K.); udaka@kochi-u.ac.jp (K.U.) 6 Department of Interdisciplinary Science and Engineering in Health Systems, Okayama University, Okayama 700-8530, Japan; futamij@okayama-u.ac.jp 2 Department of Pathology, Sapporo Medical University, Sapporo 060-8556, Japan; kanaseki@sapmed.ac.jp (T.K.); st.tokita@gmail.com (S.T.); torigoe@sapmed.ac.jp (T.T.) 1 Department of Immunotherapeutics, The University of Tokyo Hospital, Tokyo 113-8655, Japan; knagaoka@m.u-tokyo.ac.jp (K.N.); sonc-sur@h.u-tokyo.ac.jp (C.S.); yukkoba@m.u-tokyo.ac.jp (Y.K.) 7 Department of Gastrointestinal Surgery, Graduate School of Medicine, The University of Tokyo, Tokyo 113-8655, Japan; snomura-gi@umin.ac.jp 5 RIKEN Center for Integrative Medical Sciences, Laboratory for Cancer Genomics, Yokohama 230-0045, Japan; kazuhiro.maejima@riken.jp (K.M.); hidewaki@riken.jp (H.N.) |
AuthorAffiliation_xml | – name: 2 Department of Pathology, Sapporo Medical University, Sapporo 060-8556, Japan; kanaseki@sapmed.ac.jp (T.K.); st.tokita@gmail.com (S.T.); torigoe@sapmed.ac.jp (T.T.) – name: 6 Department of Interdisciplinary Science and Engineering in Health Systems, Okayama University, Okayama 700-8530, Japan; futamij@okayama-u.ac.jp – name: 4 Department of Immunology, Kochi University, Kochi 783-8505, Japan; tkomatsu@kochi-u.ac.jp (T.K.); udaka@kochi-u.ac.jp (K.U.) – name: 5 RIKEN Center for Integrative Medical Sciences, Laboratory for Cancer Genomics, Yokohama 230-0045, Japan; kazuhiro.maejima@riken.jp (K.M.); hidewaki@riken.jp (H.N.) – name: 3 Sapporo Dohto Hospital, Sapporo 065-0017, Japan – name: 7 Department of Gastrointestinal Surgery, Graduate School of Medicine, The University of Tokyo, Tokyo 113-8655, Japan; snomura-gi@umin.ac.jp – name: 1 Department of Immunotherapeutics, The University of Tokyo Hospital, Tokyo 113-8655, Japan; knagaoka@m.u-tokyo.ac.jp (K.N.); sonc-sur@h.u-tokyo.ac.jp (C.S.); yukkoba@m.u-tokyo.ac.jp (Y.K.) |
Author_xml | – sequence: 1 givenname: Koji orcidid: 0000-0001-8202-031X surname: Nagaoka fullname: Nagaoka, Koji organization: Department of Immunotherapeutics, The University of Tokyo Hospital, Tokyo 113-8655, Japan – sequence: 2 givenname: Changbo surname: Sun fullname: Sun, Changbo organization: Department of Immunotherapeutics, The University of Tokyo Hospital, Tokyo 113-8655, Japan – sequence: 3 givenname: Yukari orcidid: 0000-0002-2600-2181 surname: Kobayashi fullname: Kobayashi, Yukari organization: Department of Immunotherapeutics, The University of Tokyo Hospital, Tokyo 113-8655, Japan – sequence: 4 givenname: Takayuki surname: Kanaseki fullname: Kanaseki, Takayuki organization: Department of Pathology, Sapporo Medical University, Sapporo 060-8556, Japan – sequence: 5 givenname: Serina surname: Tokita fullname: Tokita, Serina organization: Sapporo Dohto Hospital, Sapporo 065-0017, Japan – sequence: 6 givenname: Toshihiro surname: Komatsu fullname: Komatsu, Toshihiro organization: Department of Immunology, Kochi University, Kochi 783-8505, Japan – sequence: 7 givenname: Kazuhiro surname: Maejima fullname: Maejima, Kazuhiro organization: RIKEN Center for Integrative Medical Sciences, Laboratory for Cancer Genomics, Yokohama 230-0045, Japan – sequence: 8 givenname: Junichiro orcidid: 0000-0002-0020-2855 surname: Futami fullname: Futami, Junichiro organization: Department of Interdisciplinary Science and Engineering in Health Systems, Okayama University, Okayama 700-8530, Japan – sequence: 9 givenname: Sachiyo orcidid: 0000-0003-4293-6205 surname: Nomura fullname: Nomura, Sachiyo organization: Department of Gastrointestinal Surgery, Graduate School of Medicine, The University of Tokyo, Tokyo 113-8655, Japan – sequence: 10 givenname: Keiko surname: Udaka fullname: Udaka, Keiko organization: Department of Immunology, Kochi University, Kochi 783-8505, Japan – sequence: 11 givenname: Hidewaki orcidid: 0000-0003-1807-772X surname: Nakagawa fullname: Nakagawa, Hidewaki organization: RIKEN Center for Integrative Medical Sciences, Laboratory for Cancer Genomics, Yokohama 230-0045, Japan – sequence: 12 givenname: Toshihiko orcidid: 0000-0002-9463-5917 surname: Torigoe fullname: Torigoe, Toshihiko organization: Department of Pathology, Sapporo Medical University, Sapporo 060-8556, Japan – sequence: 13 givenname: Kazuhiro orcidid: 0000-0003-2631-3040 surname: Kakimi fullname: Kakimi, Kazuhiro organization: Department of Immunotherapeutics, The University of Tokyo Hospital, Tokyo 113-8655, Japan |
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CitedBy_id | crossref_primary_10_1002_ijc_34382 crossref_primary_10_3390_cancers14225641 crossref_primary_10_3389_or_2023_12189 crossref_primary_10_1016_j_meomic_2023_100025 crossref_primary_10_1007_s10120_024_01514_5 crossref_primary_10_1172_JCI176740 |
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Keywords | adoptive cell therapy (ACT) neoantigen DC vaccine gastric cancer checkpoint inhibitor |
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Snippet | To develop combination immunotherapies for gastric cancers, immunologically well-characterized preclinical models are crucial. Here, we leveraged two... Simple SummaryDespite the success of immune checkpoint inhibitors (ICI) for treating a variety of solid cancers, most gastric cancer patients are resistant to... |
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StartPage | 106 |
SubjectTerms | Adoptive transfer Cancer therapies CD8 antigen CTLA-4 protein Dendritic cells Gastric cancer Gene expression Immune checkpoint inhibitors Immunotherapy Lymphocytes T Major histocompatibility complex Monoclonal antibodies Mutation Neoantigens PD-1 protein PD-L1 protein Peptides Tumor cell lines Tumor cells |
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Title | Identification of Neoantigens in Two Murine Gastric Cancer Cell Lines Leading to the Neoantigen-Based Immunotherapy |
URI | https://www.ncbi.nlm.nih.gov/pubmed/35008270 https://www.proquest.com/docview/2618204735 https://search.proquest.com/docview/2618898717 https://pubmed.ncbi.nlm.nih.gov/PMC8750027 |
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