Ansell SM, Lesokhin AM, Borrello I, Halwani A, Scott EC, Gutierrez M, et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin’s lymphoma. N Engl J Med. 2015;372:311–9.

Article  PubMed  Google Scholar 

Chen R, Zinzani PL, Lee HJ, Armand P, Johnson NA, Brice P, et al. Pembrolizumab in relapsed or refractory Hodgkin lymphoma: 2-year follow-up of KEYNOTE-087. Blood. 2019;134:1144–53.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Ansell SM, Minnema MC, Johnson P, Timmerman JM, Armand P, Shipp MA, et al. Nivolumab for relapsed/refractory diffuse large B-cell lymphoma in patients ineligible for or having failed autologous transplantation: a single-arm, phase II study. J Clin Oncol. 2019;37:481–9.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Lesokhin AM, Ansell SM, Armand P, Scott EC, Halwani A, Gutierrez M, et al. Nivolumab in patients with relapsed or refractory hematologic malignancy: preliminary results of a phase Ib study. J Clin Oncol. 2016;34:2698–704.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Ding W, LaPlant BR, Call TG, Parikh SA, Leis JF, He R, et al. Pembrolizumab in patients with CLL and Richter transformation or with relapsed CLL. Blood. 2017;129:3419–27.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Najafi S, Mirshafiey A. The role of T helper 17 and regulatory T cells in tumor microenvironment. Immunopharmacol Immunotoxicol. 2019;41:16–24.

Article  CAS  PubMed  Google Scholar 

Yang ZZ, Novak AJ, Ziesmer SC, Witzig TE, Ansell SM. Malignant B cells skew the balance of regulatory T cells and TH17 cells in B-cell non-Hodgkin’s lymphoma. Cancer Res. 2009;69:5522–30.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Yang ZZ, Grote DM, Xiu B, Ziesmer SC, Price-Troska TL, Hodge LS, et al. TGF-beta upregulates CD70 expression and induces exhaustion of effector memory T cells in B-cell non-Hodgkin’s lymphoma. Leukemia. 2014;28:1872–84.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Jiang Y, Li Y, Zhu B. T-cell exhaustion in the tumor microenvironment. Cell Death Dis. 2015;6:e1792.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Yang ZZ, Grote DM, Ziesmer SC, Niki T, Hirashima M, Novak AJ, et al. IL-12 upregulates TIM-3 expression and induces T cell exhaustion in patients with follicular B cell non-Hodgkin lymphoma. J Clin Invest. 2012;122:1271–82.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Yang ZZ, Kim HJ, Villasboas JC, Chen YP, Price-Troska T, Jalali S, et al. Expression of LAG-3 defines exhaustion of intratumoral PD-1(+) T cells and correlates with poor outcome in follicular lymphoma. Oncotarget. 2017;8:61425–39.

Article  PubMed  PubMed Central  Google Scholar 

Bonfiglio F, Bruscaggin A, Guidetti F, Terzi di Bergamo L, Faderl M, Spina V, et al. Genetic and phenotypic attributes of splenic marginal zone lymphoma. Blood. 2022;139:732–47.

Article  CAS  PubMed  Google Scholar 

Gallimore A, Glithero A, Godkin A, Tissot AC, Pluckthun A, Elliott T, et al. Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes. J Exp Med. 1998;187:1383–93.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Zajac AJ, Blattman JN, Murali-Krishna K, Sourdive DJ, Suresh M, Altman JD, et al. Viral immune evasion due to persistence of activated T cells without effector function. J Exp Med. 1998;188:2205–13.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Day CL, Kaufmann DE, Kiepiela P, Brown JA, Moodley ES, Reddy S, et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature. 2006;443:350–4.

Article  CAS  PubMed  Google Scholar 

D’Souza M, Fontenot AP, Mack DG, Lozupone C, Dillon S, Meditz A, et al. Programmed death 1 expression on HIV-specific CD4+ T cells is driven by viral replication and associated with T cell dysfunction. J Immunol. 2007;179:1979–87.

Article  PubMed  Google Scholar 

Jin HT, Anderson AC, Tan WG, West EE, Ha SJ, Araki K, et al. Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc Natl Acad Sci USA. 2010;107:14733–8.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Takamura S, Tsuji-Kawahara S, Yagita H, Akiba H, Sakamoto M, Chikaishi T, et al. Premature terminal exhaustion of Friend virus-specific effector CD8+ T cells by rapid induction of multiple inhibitory receptors. J Immunol. 2010;184:4696–707.

Article  CAS  PubMed  Google Scholar 

Grosso JF, Goldberg MV, Getnet D, Bruno TC, Yen HR, Pyle KJ, et al. Functionally distinct LAG-3 and PD-1 subsets on activated and chronically stimulated CD8 T cells. J Immunol. 2009;182:6659–69.

Article  CAS  PubMed  Google Scholar 

Zhou Q, Munger ME, Veenstra RG, Weigel BJ, Hirashima M, Munn DH, et al. Coexpression of Tim-3 and PD-1 identifies a CD8+ T-cell exhaustion phenotype in mice with disseminated acute myelogenous leukemia. Blood. 2011;117:4501–10.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Matsuzaki J, Gnjatic S, Mhawech-Fauceglia P, Beck A, Miller A, Tsuji T, et al. Tumor-infiltrating NY-ESO-1-specific CD8+ T cells are negatively regulated by LAG-3 and PD-1 in human ovarian cancer. Proc Natl Acad Sci USA. 2010;107:7875–80.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Johnston RJ, Comps-Agrar L, Hackney J, Yu X, Huseni M, Yang Y, et al. The immunoreceptor TIGIT regulates antitumor and antiviral CD8(+) T cell effector function. Cancer Cell. 2014;26:923–37.

Article  CAS  PubMed  Google Scholar 

Chauvin JM, Pagliano O, Fourcade J, Sun Z, Wang H, Sander C, et al. TIGIT and PD-1 impair tumor antigen-specific CD8(+) T cells in melanoma patients. J Clin Invest. 2015;125:2046–58.

Article  PubMed  PubMed Central  Google Scholar 

Yang ZZ, Grote DM, Ziesmer SC, Xiu B, Novak AJ, Ansell SM. PD-1 expression defines two distinct T-cell sub-populations in follicular lymphoma that differentially impact patient survival. Blood Cancer J. 2015;5:e281.

Article  PubMed  PubMed Central  Google Scholar 

Yang ZZ, Kim HJ, Villasboas JC, Price-Troska T, Jalali S, Wu H, et al. Mass cytometry analysis reveals that specific intratumoral CD4(+) T cell subsets correlate with patient survival in follicular lymphoma. Cell Rep. 2019;26:2178–2193.e2173.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Kotecha N, Krutzik PO, Irish JM. Web-based analysis and publication of flow cytometry experiments. Curr Protoc Cytom. 2010;Chapter 10:Unit10 17.

PubMed  Google Scholar 

Nowicka M, Krieg C, Crowell HL, Weber LM, Hartmann FJ, Guglietta S, et al. CyTOF workflow: differential discovery in high-throughput high-dimensional cytometry datasets. F1000Res. 2017;6:748.

Article  PubMed  Google Scholar 

Bengsch B, Ohtani T, Khan O, Setty M, Manne S, O’Brien S, et al. Epigenomic-guided mass cytometry profiling reveals disease-specific features of exhausted CD8 T cells. Immunity. 2018;48:1029–1045.e1025.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Maurer MJ, Ghesquieres H, Jais JP, Witzig TE, Haioun C, Thompson CA, et al. Event-free survival at 24 months is a robust end point for disease-related outcome in diffuse large B-cell lymphoma treated with immunochemotherapy. J Clin Oncol. 2014;32:1066–73.

Article  PubMed  PubMed Central  Google Scholar 

Audia S, Rossato M, Santegoets K, Spijkers S, Wichers C, Bekker C, et al. Splenic TFH expansion participates in B-cell differentiation and antiplatelet-antibody production during immune thrombocytopenia. Blood. 2014;124:2858–66.

Article  CAS  PubMed  Google Scholar 

Ame-Thomas P, Le Priol J, Yssel H, Caron G, Pangault C, Jean R, et al. Characterization of intratumoral follicular helper T cells in follicular lymphoma: role in the survival of malignant B cells. Leukemia. 2012;26:1053–63.

Article  CAS  PubMed  Google Scholar 

Sugimoto T, Watanabe T. Follicular lymphoma: the role of the tumor microenvironment in prognosis. J Clin Exp Hematop. 2016;56:1–19.

Article  PubMed  PubMed Central  Google Scholar 

Audia S, Rossato M, Trad M, Samson M, Santegoets K, Gautheron A, et al. B cell depleting therapy regulates splenic and circulating T follicular helper cells in immune thrombocytopenia. J Autoimmun. 2017;77:89–95.

Article  CAS  PubMed  Google Scholar 

Zhao J, Shi J, Qu M, Zhao X, Wang H, Huang M, et al. Hyperactive follicular helper T cells contribute to dysregulated humoral immunity in patients with liver cirrhosis. Front Immunol. 2019;10:1915.

Article  CAS  PubMed