γδ T Cells in Merkel Cell Carcinomas Have a Proinflammatory Profile Prognostic of Patient Survival.

Adult Aged Aged, 80 and over Biomarkers CD4-Positive T-Lymphocytes / immunology CD8-Positive T-Lymphocytes / immunology Carcinoma, Merkel Cell / drug therapy Cell Line Computational Biology Female Humans Immune Checkpoint Inhibitors / therapeutic use Male Middle Aged Prognosis Receptors, Antigen, T-Cell, gamma-delta / immunology Skin Neoplasms / drug therapy Survival Analysis T-Lymphocytes / immunology

Journal

Cancer immunology research

ISSN: 2326-6074

Titre abrégé: Cancer Immunol Res

Pays: United States

ID NLM: 101614637

Informations de publication

Date de publication:
06 2021

Historique:

received: 01 10 2020

revised: 14 01 2021

accepted: 03 03 2021

pubmed: 7 3 2021

medline: 21 1 2022

entrez: 6 3 2021

Statut: ppublish

Résumé

Merkel cell carcinomas (MCC) are immunogenic skin cancers associated with viral infection or UV mutagenesis. To study T-cell infiltrates in MCC, we analyzed 58 MCC lesions from 39 patients using multiplex-IHC/immunofluorescence (m-IHC/IF). CD4

Identifiants

DOI: 10.1158/2326-6066.CIR-20-0817 PMID: 33674358

pubmed: 33674358

pii: 2326-6066.CIR-20-0817

doi: 10.1158/2326-6066.CIR-20-0817

doi:

Substances chimiques

Biomarkers 0

Immune Checkpoint Inhibitors 0

Receptors, Antigen, T-Cell, gamma-delta 0

Types de publication

Journal Article Multicenter Study Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

Pagination

612-623

Commentaires et corrections

Type : CommentIn

Informations de copyright

Références

Shuda M, Feng H, Kwun HJ, Rosen ST, Gjoerup O, Moore PS, et al. T antigen mutations are a human tumor-specific signature for Merkel cell polyomavirus. Proc Natl Acad Sci U S A. 2008;105:16272–7.

Houben R, Shuda M, Weinkam R, Schrama D, Feng H, Chang Y, et al. Merkel cell polyomavirus-infected Merkel cell carcinoma cells require expression of viral T antigens. J Virol. 2010;84:7064–72.

Harms PW, Vats P, Verhaegen ME, Robinson DR, Wu YM, Dhanasekaran SM, et al. The distinctive mutational spectra of polyomavirus-negative Merkel cell carcinoma. Cancer Res. 2015;75:3720–7.

Wong SQ, Waldeck K, Vergara IA, Schroder J, Madore J, Wilmott JS, et al. UV-associated mutations underlie the etiology of MCV-negative Merkel cell carcinomas. Cancer Res. 2015;75:5228–34.

Goh G, Walradt T, Markarov V, Blom A, Riaz N, Doumani R, et al. Mutational landscape of MCPyV-positive and MCPyV-negative Merkel cell carcinomas with implications for immunotherapy. Oncotarget. 2016;7:3403–15.

Walsh NM. Complete spontaneous regression of Merkel cell carcinoma (1986–2016): a 30 year perspective. J Cutan Pathol. 2016;43:1150–4.

Vandeven N, Lewis CW, Makarov V, Riaz N, Paulson KG, Hippe D, et al. Merkel cell carcinoma patients presenting without a primary lesion have elevated markers of immunity, higher tumor mutation burden, and improved survival. Clin Cancer Res. 2018;24:963–71.

Kaufman HL, Russell J, Hamid O, Bhatia S, Terheyden P, D'Angelo SP, et al. Avelumab in patients with chemotherapy-refractory metastatic Merkel cell carcinoma: a multicentre, single-group, open-label, phase 2 trial. Lancet Oncol. 2016;17:1374–85.

Nghiem P, Bhatia S, Lipson EJ, Sharfman WH, Kudchadkar RR, Brohl AS, et al. Durable tumor regression and overall survival in patients with advanced Merkel cell carcinoma receiving pembrolizumab as first-line therapy. J Clin Oncol. 2019;37:693–702.

Walker JW, Lebbe C, Grignani G, Nathan P, Dirix L, Fenig E, et al. Efficacy and safety of avelumab treatment in patients with metastatic Merkel cell carcinoma: experience from a global expanded access program. J Immunother Cancer. 2020;8:e000313.

Paulson KG, Iyer JG, Tegeder AR, Thibodeau R, Schelter J, Koba S, et al. Transcriptome-wide studies of merkel cell carcinoma and validation of intratumoral CD8+ lymphocyte invasion as an independent predictor of survival. J Clin Oncol. 2011;29:1539–46.

Sihto H, Böhling T, Kavola H, Koljonen V, Salmi M, Jalkanen S, et al. Tumor infiltrating immune cells and outcome of Merkel cell carcinoma: a population-based study. Clin Cancer Res. 2012;18:2872–81.

Paulson KG, Iyer JG, Simonson WT, Blom A, Thibodeau RM, Schmidt M, et al. CD8+ lymphocyte intratumoral infiltration as a stage-independent predictor of merkel cell carcinoma survival: a population-based study. Am J Clin Pathol. 2014;142:452–8.

Iyer JG, Afanasiev OK, McClurkan C, Paulson K, Nagase K, Jing L, et al. Merkel cell polyomavirus-specific CD8(+) and CD4(+) T-cell responses identified in Merkel cell carcinomas and blood. Clin Cancer Res. 2011;17:6671–80.

Afanasiev OK, Yelistratova L, Miller N, Nagase K, Paulson K, Iyer JG, et al. Merkel polyomavirus-specific T cells fluctuate with merkel cell carcinoma burden and express therapeutically targetable PD-1 and Tim-3 exhaustion markers. Clin Cancer Res. 2013;19:5351–60.

Lyngaa R, Pedersen NW, Schrama D, Thrue CA, Ibrani D, Met O, et al. T-cell responses to oncogenic merkel cell polyomavirus proteins distinguish patients with merkel cell carcinoma from healthy donors. Clin Cancer Res. 2014;20:1768–78.

Miller NJ, Church CD, Dong L, Crispin D, Fitzgibbon MP, Lachance K, et al. Tumor-infiltrating merkel cell polyomavirus-specific T cells are diverse and associated with improved patient survival. Cancer Immunol Res. 2017;;5:137–47.

Paulson KG, Tegeder A, Willmes C, Iyer JG, Afanasiev OK, Schrama D, et al. Downregulation of MHC-I expression is prevalent but reversible in Merkel cell carcinoma. Cancer Immunol Res. 2014;2:1071–9.

Paulson KG, Voillet V, McAfee MS, Hunter DS, Wagener FD, Perdicchio M, et al. Acquired cancer resistance to combination immunotherapy from transcriptional loss of class I HLA. Nat Commun. 2018;9:3868.

Godfrey DI, Uldrich AP, McCluskey J, Rossjohn J, Moody DB. The burgeoning family of unconventional T cells. Nat Immunol. 2015;16:1114–23.

Girard P, Charles J, Cluzel C, Degeorges E, Manches O, Plumas J, et al. The features of circulating and tumor-infiltrating gammadelta T cells in melanoma patients display critical perturbations with prognostic impact on clinical outcome. Oncoimmunology. 2019;8:1601483.

Wistuba-Hamprecht K, Martens A, Haehnel K, Geukes Foppen M, Yuan J, Postow MA, et al. Proportions of blood-borne Vdelta1+ and Vdelta2+ T-cells are associated with overall survival of melanoma patients treated with ipilimumab. Eur J Cancer. 2016;64:116–26.

Lo Presti E, Toia F, Oieni S, Buccheri S, Turdo A, Mangiapane LR, et al. Squamous cell tumors recruit gammadelta T cells producing either IL17 or IFNgamma depending on the tumor stage. Cancer Immunol Res. 2017;5:397–407.

Ma C, Zhang Q, Ye J, Wang F, Zhang Y, Wevers E, et al. Tumor-infiltrating gammadelta T lymphocytes predict clinical outcome in human breast cancer. J Immunol. 2012;189:5029–36.

Meraviglia S, Lo Presti E, Tosolini M, La Mendola C, Orlando V, Todaro M, et al. Distinctive features of tumor-infiltrating gammadelta T lymphocytes in human colorectal cancer. Oncoimmunology. 2017;6:e1347742.

Wu P, Wu D, Ni C, Ye J, Chen W, Hu G, et al. gammadeltaT17 cells promote the accumulation and expansion of myeloid-derived suppressor cells in human colorectal cancer. Immunity. 2014;40:785–800.

Daley D, Zambirinis CP, Seifert L, Akkad N, Mohan N, Werba G, et al. gammadelta T cells support pancreatic oncogenesis by restraining alphabeta T cell activation. Cell. 2016;166:1485–99.

Guo XZ, Dash P, Calverley M, Tomchuck S, Dallas MH, Thomas PG. Rapid cloning, expression, and functional characterization of paired alphabeta and gammadelta T-cell receptor chains from single-cell analysis. Mol Ther Methods Clin Dev. 2016;3:15054.

Weppler A, Pattison A, Weppler AM, Bhave P, De Ieso PB, et al. Clinical, FDG-PET and molecular markers of immune checkpoint inhibitor response in patients with metastatic merkel cell carcinoma. J Immunother Cancer. 2020;8:e00070.

Park DE, Cheng J, McGrath JP, Lim MY, Cushman C, Swanson SK, et al. Merkel cell polyomavirus activates LSD1-mediated blockade of non-canonical BAF to regulate transformation and tumorigenesis. Nat Cell Biol. 2020;22:603–15.

Gutierrez-Arcelus M, Teslovich N, Mola AR, Polidoro RB, Nathan A, Kim H, et al. Lymphocyte innateness defined by transcriptional states reflects a balance between proliferation and effector functions. Nat Commun. 2019;10:687.

Le Nours J, Gherardin NA, Ramarathinam SH, Awad W, Wiede F, Gully BS, et al. A class of gammadelta T cell receptors recognize the underside of the antigen-presenting molecule MR1. Science. 2019;366:1522–7.

Holst J, Szymczak-Workman AL, Vignali KM, Burton AR, Workman CJ, Vignali DA. Generation of T-cell receptor retrogenic mice. Nat Protoc. 2006;1:406–17.

Gherardin NA, Keller AN, Woolley RE, Le Nours J, Ritchie DS, Neeson PJ, et al. Diversity of T cells restricted by the MHC class I-related molecule MR1 facilitates differential antigen recognition. Immunity. 2016;44:32–45.

Birkinshaw RW, Pellicci DG, Cheng TY, Keller AN, Sandoval-Romero M, Gras S, et al. alphabeta T cell antigen receptor recognition of CD1a presenting self lipid ligands. Nat Immunol. 2015;16:258–66.

James CA, Yu KKQ, Gilleron M, Prandi J, Yedulla VR, Moleda ZZ, et al. CD1b tetramers identify T cells that recognize natural and synthetic diacylated sulfoglycolipids from mycobacterium tuberculosis. Cell Chem Biol. 2018;25:392–402.

Wun KS, Reijneveld JF, Cheng TY, Ladell K, Uldrich AP, Nours Le, et al. T cell autoreactivity directed toward CD1c itself rather than toward carried self lipids. Nat Immunol. 2018;19:397–406.

Uldrich AP, Patel O, Cameron G, Pellicci DG, Day EB, Sullivan LC, et al. A semi-invariant Valpha10+ T cell antigen receptor defines a population of natural killer T cells with distinct glycolipid antigen-recognition properties. Nat Immunol. 2011;12:616–23.

Dusseaux M, Martin E, Serriari N, Peguillet I, Premel V, Louis D, et al. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood. 2011;117:1250–9.

Cordova A, Toia F, La Mendola C, Orlando V, Meraviglia S, Rinaldi G, et al. Characterization of human gammadelta T lymphocytes infiltrating primary malignant melanomas. PLoS One. 2012;7:e49878.

Gentles AJ, Newman AM, Liu CL, Bratman SV, Feng W, Kim D, et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med. 2015;21:938–45.

Tosolini M, Pont F, Poupot M, Vergez F, Nicolau-Travers ML, Vermijlen D, et al. Assessment of tumor-infiltrating TCRVgamma9Vdelta2 gammadelta lymphocyte abundance by deconvolution of human cancers microarrays. Oncoimmunology. 2017;6:e1284723.

Pizzolato G, Kaminski H, Tosolini M, Franchini DM, Pont F, Martins F, et al. Single-cell RNA sequencing unveils the shared and the distinct cytotoxic hallmarks of human TCRVδ1 and TCRVδ2 γδ T lymphocytes. Proc Natl Acad Sci U S A. 2019;;116:11906–15.

Laniosz V, Onajin O, Sominidi-Damodaran S, Meves A, Gibson LE, Baum CL. Natural killer cell response is a predictor of good outcome in MCPyV+ Merkel cell carcinoma: a case series of 23 patients. J Am Acad Dermatol. 2017;;7:31–2.

Couzi L, Pitard V, Sicard X, Garrigue I, Hawchar O, Merville P, et al. Antibody-dependent anti-cytomegalovirus activity of human gammadelta T cells expressing CD16 (FcgammaRIIIa). Blood. 2012;119:1418–27.

Lepore M, de Lalla C, Gundimeda SR, Gsellinger H, Consonni M, Garavaglia C, et al. A novel self-lipid antigen targets human T cells against CD1c(+) leukemias. J Exp Med. 2014;211:1363–77.

Crowther MD, Dolton G, Legut M, Caillaud ME, Lloyd A, Attaf M, et al. Genome-wide CRISPR-Cas9 screening reveals ubiquitous T cell cancer targeting via the monomorphic MHC class I-related protein MR1. Nat Immunol. 2020;21:178–85.

Lepore M, Kalinichenko A, Calogero S, Kumar P, Paleja B, Schmaler M, et al. Functionally diverse human T cells recognize non-microbial antigens presented by MR1. Elife. 2017;6:e24476.

Hoeres T, Holzmann E, Smetak M, Birkmann J, Wilhelm M. PD-1 signaling modulates interferon-gamma production by gamma delta (gammadelta) T-cells in response to leukemia. Oncoimmunology. 2019;8:1550618.

Silva-Santos B, Mensurado S, Coffelt SB. gammadelta T cells: pleiotropic immune effectors with therapeutic potential in cancer. Nat Rev Cancer. 2019;;19:392–404.