Baseline and post-treatment biomarkers of resistance to anti-PD-1 therapy in acral and mucosal melanoma: an observational study

BackgroundImmunotherapies targeting programmed cell death-1 (PD-1) and its ligands have improved clinical outcomes for advanced melanoma. However, many tumors exhibit primary resistance or acquire secondary resistance after an initial positive response. The mechanisms of resistance are not well unde...

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Vydáno v:	Journal for immunotherapy of cancer Ročník 10; číslo 7; s. e004879
Hlavní autoři:	Shui, Irene M., Liu, Xiao Qiao, Zhao, Qing, Kim, Seung Tae, Sun, Yuan, Yearley, Jennifer H., Choudhury, Tasmiah, Webber, Andrea L., Krepler, Clemens, Cristescu, Razvan, Lee, Jeeyun
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	England BMJ Publishing Group Ltd 01.07.2022 BMJ Publishing Group LTD BMJ Publishing Group
Edice:	Original research
Témata:	Antigen presentation Apoptosis Biomarkers Biomarkers - analysis Biomarkers, Tumor Cancer Cell death Clinical outcomes Gene expression Humans Immunotherapy Immunotherapy Biomarkers Kinases Melanoma Melanoma - immunology Melanoma - pathology Melanoma - therapy Metastasis Mutation Observational studies Programmed Cell Death 1 Receptor Programmed Cell Death 1 Receptor - antagonists & inhibitors Programmed Cell Death 1 Receptor - immunology Retrospective Studies RNA, Messenger - biosynthesis Tumors Programmed Cell Death 1 Receptor Biomarkers, Tumor Melanoma
ISSN:	2051-1426, 2051-1426
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Abstract	BackgroundImmunotherapies targeting programmed cell death-1 (PD-1) and its ligands have improved clinical outcomes for advanced melanoma. However, many tumors exhibit primary resistance or acquire secondary resistance after an initial positive response. The mechanisms of resistance are not well understood, and no validated predictive biomarkers are available. This exploratory study aimed to characterize baseline differences and molecular changes arising during treatment in acral and mucosal melanomas that exhibited primary or secondary resistance to anti-PD-1 monotherapy.MethodsThis was an observational retrospective study of 124 patients who had been treated for metastatic acral or mucosal melanoma with anti-PD-1 monotherapy. Tumor samples were collected at baseline (all patients) and post-treatment (resistant tumors only) and were assayed by immunohistochemistry, whole-exome sequencing, and RNA sequencing.ResultsAt baseline, more non-progressor than resistant tumors exhibited expression of PD-L1, immune cell infiltration, and high tumor mutational burden (TMB); baseline PD-L1 expression was also more common in secondary-resistant than in primary-resistant tumors as well as in late versus early secondary-resistant tumors. Non-progressor tumors also had higher median baseline expression of an 18-gene T cell-inflamed gene expression profile (TcellinfGEP). Among resistant tumors, the proportion of PD-L1-positive melanomas and the expression of the TcellinfGEP mRNA signature increased during treatment, while the expression of mRNA signatures related to WNT and INFA1 signaling decreased. There was evidence for greater changes from baseline in secondary-resistant versus primary-resistant tumors for some markers, including expression of RAS-related and WNT-related mRNA signatures and density of CD11c+ and FOXP3+ T cells. Greater changes in CD11c+ cell density were observed in early compared with late secondary-resistant tumors.ConclusionsOur findings suggest that TcellinfGEP and PD-L1 expression, TMB, immune cell infiltration, and RAS and WNT signaling warrant further investigation as potential mechanisms and/or biomarkers of anti-PD-1 therapy resistance in acral and mucosal melanomas. Confirmation of these findings in larger populations is needed.
AbstractList	BackgroundImmunotherapies targeting programmed cell death-1 (PD-1) and its ligands have improved clinical outcomes for advanced melanoma. However, many tumors exhibit primary resistance or acquire secondary resistance after an initial positive response. The mechanisms of resistance are not well understood, and no validated predictive biomarkers are available. This exploratory study aimed to characterize baseline differences and molecular changes arising during treatment in acral and mucosal melanomas that exhibited primary or secondary resistance to anti-PD-1 monotherapy.MethodsThis was an observational retrospective study of 124 patients who had been treated for metastatic acral or mucosal melanoma with anti-PD-1 monotherapy. Tumor samples were collected at baseline (all patients) and post-treatment (resistant tumors only) and were assayed by immunohistochemistry, whole-exome sequencing, and RNA sequencing.ResultsAt baseline, more non-progressor than resistant tumors exhibited expression of PD-L1, immune cell infiltration, and high tumor mutational burden (TMB); baseline PD-L1 expression was also more common in secondary-resistant than in primary-resistant tumors as well as in late versus early secondary-resistant tumors. Non-progressor tumors also had higher median baseline expression of an 18-gene T cell-inflamed gene expression profile (TcellinfGEP). Among resistant tumors, the proportion of PD-L1-positive melanomas and the expression of the TcellinfGEP mRNA signature increased during treatment, while the expression of mRNA signatures related to WNT and INFA1 signaling decreased. There was evidence for greater changes from baseline in secondary-resistant versus primary-resistant tumors for some markers, including expression of RAS-related and WNT-related mRNA signatures and density of CD11c+ and FOXP3+ T cells. Greater changes in CD11c+ cell density were observed in early compared with late secondary-resistant tumors.ConclusionsOur findings suggest that TcellinfGEP and PD-L1 expression, TMB, immune cell infiltration, and RAS and WNT signaling warrant further investigation as potential mechanisms and/or biomarkers of anti-PD-1 therapy resistance in acral and mucosal melanomas. Confirmation of these findings in larger populations is needed. Immunotherapies targeting programmed cell death-1 (PD-1) and its ligands have improved clinical outcomes for advanced melanoma. However, many tumors exhibit primary resistance or acquire secondary resistance after an initial positive response. The mechanisms of resistance are not well understood, and no validated predictive biomarkers are available. This exploratory study aimed to characterize baseline differences and molecular changes arising during treatment in acral and mucosal melanomas that exhibited primary or secondary resistance to anti-PD-1 monotherapy. This was an observational retrospective study of 124 patients who had been treated for metastatic acral or mucosal melanoma with anti-PD-1 monotherapy. Tumor samples were collected at baseline (all patients) and post-treatment (resistant tumors only) and were assayed by immunohistochemistry, whole-exome sequencing, and RNA sequencing. At baseline, more non-progressor than resistant tumors exhibited expression of PD-L1, immune cell infiltration, and high tumor mutational burden (TMB); baseline PD-L1 expression was also more common in secondary-resistant than in primary-resistant tumors as well as in late versus early secondary-resistant tumors. Non-progressor tumors also had higher median baseline expression of an 18-gene T cell-inflamed gene expression profile (Tcell GEP). Among resistant tumors, the proportion of PD-L1-positive melanomas and the expression of the Tcell GEP mRNA signature increased during treatment, while the expression of mRNA signatures related to WNT and INFA1 signaling decreased. There was evidence for greater changes from baseline in secondary-resistant versus primary-resistant tumors for some markers, including expression of RAS-related and WNT-related mRNA signatures and density of CD11c and FOXP3 T cells. Greater changes in CD11c cell density were observed in early compared with late secondary-resistant tumors. Our findings suggest that Tcell GEP and PD-L1 expression, TMB, immune cell infiltration, and RAS and WNT signaling warrant further investigation as potential mechanisms and/or biomarkers of anti-PD-1 therapy resistance in acral and mucosal melanomas. Confirmation of these findings in larger populations is needed. Background Immunotherapies targeting programmed cell death-1 (PD-1) and its ligands have improved clinical outcomes for advanced melanoma. However, many tumors exhibit primary resistance or acquire secondary resistance after an initial positive response. The mechanisms of resistance are not well understood, and no validated predictive biomarkers are available. This exploratory study aimed to characterize baseline differences and molecular changes arising during treatment in acral and mucosal melanomas that exhibited primary or secondary resistance to anti-PD-1 monotherapy.Methods This was an observational retrospective study of 124 patients who had been treated for metastatic acral or mucosal melanoma with anti-PD-1 monotherapy. Tumor samples were collected at baseline (all patients) and post-treatment (resistant tumors only) and were assayed by immunohistochemistry, whole-exome sequencing, and RNA sequencing.Results At baseline, more non-progressor than resistant tumors exhibited expression of PD-L1, immune cell infiltration, and high tumor mutational burden (TMB); baseline PD-L1 expression was also more common in secondary-resistant than in primary-resistant tumors as well as in late versus early secondary-resistant tumors. Non-progressor tumors also had higher median baseline expression of an 18-gene T cell-inflamed gene expression profile (TcellinfGEP). Among resistant tumors, the proportion of PD-L1-positive melanomas and the expression of the TcellinfGEP mRNA signature increased during treatment, while the expression of mRNA signatures related to WNT and INFA1 signaling decreased. There was evidence for greater changes from baseline in secondary-resistant versus primary-resistant tumors for some markers, including expression of RAS-related and WNT-related mRNA signatures and density of CD11c+ and FOXP3+ T cells. Greater changes in CD11c+ cell density were observed in early compared with late secondary-resistant tumors.Conclusions Our findings suggest that TcellinfGEP and PD-L1 expression, TMB, immune cell infiltration, and RAS and WNT signaling warrant further investigation as potential mechanisms and/or biomarkers of anti-PD-1 therapy resistance in acral and mucosal melanomas. Confirmation of these findings in larger populations is needed. Immunotherapies targeting programmed cell death-1 (PD-1) and its ligands have improved clinical outcomes for advanced melanoma. However, many tumors exhibit primary resistance or acquire secondary resistance after an initial positive response. The mechanisms of resistance are not well understood, and no validated predictive biomarkers are available. This exploratory study aimed to characterize baseline differences and molecular changes arising during treatment in acral and mucosal melanomas that exhibited primary or secondary resistance to anti-PD-1 monotherapy.BACKGROUNDImmunotherapies targeting programmed cell death-1 (PD-1) and its ligands have improved clinical outcomes for advanced melanoma. However, many tumors exhibit primary resistance or acquire secondary resistance after an initial positive response. The mechanisms of resistance are not well understood, and no validated predictive biomarkers are available. This exploratory study aimed to characterize baseline differences and molecular changes arising during treatment in acral and mucosal melanomas that exhibited primary or secondary resistance to anti-PD-1 monotherapy.This was an observational retrospective study of 124 patients who had been treated for metastatic acral or mucosal melanoma with anti-PD-1 monotherapy. Tumor samples were collected at baseline (all patients) and post-treatment (resistant tumors only) and were assayed by immunohistochemistry, whole-exome sequencing, and RNA sequencing.METHODSThis was an observational retrospective study of 124 patients who had been treated for metastatic acral or mucosal melanoma with anti-PD-1 monotherapy. Tumor samples were collected at baseline (all patients) and post-treatment (resistant tumors only) and were assayed by immunohistochemistry, whole-exome sequencing, and RNA sequencing.At baseline, more non-progressor than resistant tumors exhibited expression of PD-L1, immune cell infiltration, and high tumor mutational burden (TMB); baseline PD-L1 expression was also more common in secondary-resistant than in primary-resistant tumors as well as in late versus early secondary-resistant tumors. Non-progressor tumors also had higher median baseline expression of an 18-gene T cell-inflamed gene expression profile (TcellinfGEP). Among resistant tumors, the proportion of PD-L1-positive melanomas and the expression of the TcellinfGEP mRNA signature increased during treatment, while the expression of mRNA signatures related to WNT and INFA1 signaling decreased. There was evidence for greater changes from baseline in secondary-resistant versus primary-resistant tumors for some markers, including expression of RAS-related and WNT-related mRNA signatures and density of CD11c+ and FOXP3+ T cells. Greater changes in CD11c+ cell density were observed in early compared with late secondary-resistant tumors.RESULTSAt baseline, more non-progressor than resistant tumors exhibited expression of PD-L1, immune cell infiltration, and high tumor mutational burden (TMB); baseline PD-L1 expression was also more common in secondary-resistant than in primary-resistant tumors as well as in late versus early secondary-resistant tumors. Non-progressor tumors also had higher median baseline expression of an 18-gene T cell-inflamed gene expression profile (TcellinfGEP). Among resistant tumors, the proportion of PD-L1-positive melanomas and the expression of the TcellinfGEP mRNA signature increased during treatment, while the expression of mRNA signatures related to WNT and INFA1 signaling decreased. There was evidence for greater changes from baseline in secondary-resistant versus primary-resistant tumors for some markers, including expression of RAS-related and WNT-related mRNA signatures and density of CD11c+ and FOXP3+ T cells. Greater changes in CD11c+ cell density were observed in early compared with late secondary-resistant tumors.Our findings suggest that TcellinfGEP and PD-L1 expression, TMB, immune cell infiltration, and RAS and WNT signaling warrant further investigation as potential mechanisms and/or biomarkers of anti-PD-1 therapy resistance in acral and mucosal melanomas. Confirmation of these findings in larger populations is needed.CONCLUSIONSOur findings suggest that TcellinfGEP and PD-L1 expression, TMB, immune cell infiltration, and RAS and WNT signaling warrant further investigation as potential mechanisms and/or biomarkers of anti-PD-1 therapy resistance in acral and mucosal melanomas. Confirmation of these findings in larger populations is needed.
Author	Sun, Yuan Zhao, Qing Krepler, Clemens Yearley, Jennifer H. Cristescu, Razvan Webber, Andrea L. Lee, Jeeyun Kim, Seung Tae Shui, Irene M. Choudhury, Tasmiah Liu, Xiao Qiao
AuthorAffiliation	3 Hematology and Oncology , Samsung Medical Center , Gangnam-gu , South Korea 2 MSD China , Beijing , Shanghai , China 1 Merck & Co., Inc , Rahway , New Jersey , USA
AuthorAffiliation_xml	– name: 1 Merck & Co., Inc , Rahway , New Jersey , USA – name: 2 MSD China , Beijing , Shanghai , China – name: 3 Hematology and Oncology , Samsung Medical Center , Gangnam-gu , South Korea
Author_xml	– sequence: 1 givenname: Irene M. orcidid: 0000-0001-5737-9830 surname: Shui fullname: Shui, Irene M. email: irene.shui@merck.com organization: Merck & Co., Inc, Rahway, New Jersey, USA – sequence: 2 givenname: Xiao Qiao surname: Liu fullname: Liu, Xiao Qiao organization: MSD China, Beijing, Shanghai, China – sequence: 3 givenname: Qing surname: Zhao fullname: Zhao, Qing organization: Merck & Co., Inc, Rahway, New Jersey, USA – sequence: 4 givenname: Seung Tae surname: Kim fullname: Kim, Seung Tae organization: Hematology and Oncology, Samsung Medical Center, Gangnam-gu, South Korea – sequence: 5 givenname: Yuan surname: Sun fullname: Sun, Yuan organization: Merck & Co., Inc, Rahway, New Jersey, USA – sequence: 6 givenname: Jennifer H. surname: Yearley fullname: Yearley, Jennifer H. organization: Merck & Co., Inc, Rahway, New Jersey, USA – sequence: 7 givenname: Tasmiah surname: Choudhury fullname: Choudhury, Tasmiah organization: Merck & Co., Inc, Rahway, New Jersey, USA – sequence: 8 givenname: Andrea L. surname: Webber fullname: Webber, Andrea L. organization: Merck & Co., Inc, Rahway, New Jersey, USA – sequence: 9 givenname: Clemens surname: Krepler fullname: Krepler, Clemens organization: Merck & Co., Inc, Rahway, New Jersey, USA – sequence: 10 givenname: Razvan surname: Cristescu fullname: Cristescu, Razvan organization: Merck & Co., Inc, Rahway, New Jersey, USA – sequence: 11 givenname: Jeeyun surname: Lee fullname: Lee, Jeeyun organization: Hematology and Oncology, Samsung Medical Center, Gangnam-gu, South Korea
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/35793874$$D View this record in MEDLINE/PubMed
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Keywords	Programmed Cell Death 1 Receptor Biomarkers, Tumor Melanoma
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ParticipantIDs	doaj_primary_oai_doaj_org_article_7f58f81d82304caaae6769a54f66a798 pubmedcentral_primary_oai_pubmedcentral_nih_gov_9260847 proquest_miscellaneous_2686057535 proquest_journals_2686955031 pubmed_primary_35793874 crossref_primary_10_1136_jitc_2022_004879 crossref_citationtrail_10_1136_jitc_2022_004879 bmj_journals_10_1136_jitc_2022_004879
PublicationCentury	2000
PublicationDate	2022-07-01
PublicationDateYYYYMMDD	2022-07-01
PublicationDate_xml	– month: 07 year: 2022 text: 2022-07-01 day: 01
PublicationDecade	2020
PublicationPlace	England
PublicationPlace_xml	– name: England – name: London – name: BMA House, Tavistock Square, London, WC1H 9JR
PublicationSeriesTitle	Original research
PublicationTitle	Journal for immunotherapy of cancer
PublicationTitleAbbrev	J Immunother Cancer
PublicationTitleAlternate	J Immunother Cancer
PublicationYear	2022
Publisher	BMJ Publishing Group Ltd BMJ Publishing Group LTD BMJ Publishing Group
Publisher_xml	– name: BMJ Publishing Group Ltd – name: BMJ Publishing Group LTD – name: BMJ Publishing Group
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Snippet	BackgroundImmunotherapies targeting programmed cell death-1 (PD-1) and its ligands have improved clinical outcomes for advanced melanoma. However, many tumors... Immunotherapies targeting programmed cell death-1 (PD-1) and its ligands have improved clinical outcomes for advanced melanoma. However, many tumors exhibit... Background Immunotherapies targeting programmed cell death-1 (PD-1) and its ligands have improved clinical outcomes for advanced melanoma. However, many tumors...
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SubjectTerms	Antigen presentation Apoptosis Biomarkers Biomarkers - analysis Biomarkers, Tumor Cancer Cell death Clinical outcomes Gene expression Humans Immunotherapy Immunotherapy Biomarkers Kinases Melanoma Melanoma - immunology Melanoma - pathology Melanoma - therapy Metastasis Mutation Observational studies Programmed Cell Death 1 Receptor Programmed Cell Death 1 Receptor - antagonists & inhibitors Programmed Cell Death 1 Receptor - immunology Retrospective Studies RNA, Messenger - biosynthesis Tumors
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Title	Baseline and post-treatment biomarkers of resistance to anti-PD-1 therapy in acral and mucosal melanoma: an observational study
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