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Previously, we showed that tumor-specific, cytotoxic CD4+ T cells from tyrosinase-related protein 1 transgenic mice could overcome secondary resistance to recurring melanoma when anti\u2013programmed cell death 1 ligand (PD-L1) checkpoint blockade was combined with either anti\u2013lymphocyte-activated gene 3 (LAG-3) Abs or depletion of tumor-specific regulatory T (Treg) cells. In this study, we show that PD-L1 expressed by the host, not B16 melanoma, plays a major role in the early stages of exhaustion or primary resistance. We observed durable regression of melanoma in tumor-bearing PD-L1\u2212\/\u2212RAG\u2212\/\u2212 mice with transfer of naive tumor-specific CD4+ T cells. However, exhausted tumor-specific CD4+ T cells, which included tumor-specific Treg cells, failed to maintain durable regression of tumors in PD-L1\u2212\/\u2212RAG\u2212\/\u2212 mice unless tumor-specific Treg cells were eliminated, showing nonredundant pathways of resistance to immunotherapy were present. Translating these findings to a clinically relevant model of cancer immunotherapy, we unexpectedly showed that anti\u2013PD-L1 checkpoint blockade mildly improved immunotherapy with tumor-specific CD4+ T cells and irradiation in wild-type mice. Instead, anti\u2013LAG-3 checkpoint blockade, in combination with tumor-specific CD4+ T cells and irradiation, overcame primary resistance and treated established tumors resulting in fewer recurrences. Because LAG-3 negatively regulates effector T cell function and activates Treg cells, LAG-3 blockade may be more beneficial in overcoming primary resistance in combination immunotherapies using adoptive cellular therapy and irradiation than blockade of PD-L1.<\/jats:p>","DOI":"10.4049\/jimmunol.1701617","type":"journal-article","created":{"date-parts":[[2018,3,30]],"date-time":"2018-03-30T13:55:15Z","timestamp":1522418115000},"page":"3304-3311","source":"Crossref","is-referenced-by-count":12,"title":["PD-L1\u2013Independent Mechanisms Control the Resistance of Melanoma to CD4+ T Cell Adoptive Immunotherapy"],"prefix":"10.1093","volume":"200","author":[{"given":"Stephen R","family":"Goding","sequence":"first","affiliation":[{"name":"Department of Pathology, University of Maryland School of Medicine , Baltimore, MD 21201"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3743-047X","authenticated-orcid":false,"given":"Kyle A","family":"Wilson","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Maryland School of Medicine , Baltimore, MD 21201"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carolyn","family":"Rosinsky","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Maryland School of Medicine , Baltimore, MD 21201"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9439-667X","authenticated-orcid":false,"given":"Paul Andrew","family":"Antony","sequence":"additional","affiliation":[{"name":"Department of Pathology, University of Maryland School of Medicine , Baltimore, MD 21201"},{"name":"Department of Microbiology and Immunology, University of Maryland School of Medicine , Baltimore, MD 21201"},{"name":"Tumor Immunology and Immunotherapy Program, University of Maryland Cancer Center , Baltimore, MD 21201"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2018,5,1]]},"reference":[{"key":"2025030610145569400_r1","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1038\/nrclinonc.2016.36","article-title":"Driving CAR T-cells forward","volume":"13","author":"Jackson","year":"2016","journal-title":"Nat. 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