NK- and T-cell subsets in malignant mesothelioma patients: Baseline pattern and changes in the context of anti-CTLA-4 therapy.
Antibodies, Monoclonal, Humanized
/ therapeutic use
Antineoplastic Agents
/ therapeutic use
CD56 Antigen
/ immunology
CTLA-4 Antigen
/ antagonists & inhibitors
Cell Line, Tumor
Cells, Cultured
Cytokines
/ blood
Female
Gene Expression Regulation, Neoplastic
Humans
K562 Cells
Kaplan-Meier Estimate
Killer Cells, Natural
/ immunology
Lung Neoplasms
/ drug therapy
Male
Mesothelioma
/ drug therapy
Mesothelioma, Malignant
Middle Aged
Prognosis
T-Lymphocyte Subsets
/ immunology
NK cells
T cells
anti-CTLA-4 therapy
immunoprofiling
malignant mesothelioma
Journal
International journal of cancer
ISSN: 1097-0215
Titre abrégé: Int J Cancer
Pays: United States
ID NLM: 0042124
Informations de publication
Date de publication:
15 10 2019
15 10 2019
Historique:
received:
03
01
2019
accepted:
08
04
2019
pubmed:
25
4
2019
medline:
6
2
2020
entrez:
25
4
2019
Statut:
ppublish
Résumé
Malignant mesothelioma (MM) is a highly aggressive form of cancer with limited treatment options. Although the role of NK cells has been studied in many solid tumors, the pattern of NK-cell subsets and their recognition of mesothelioma cells remain to be explored. We used RNA expression data of MM biopsies derived from the cancer genome atlas to evaluate the immune cell infiltrates. We characterized the phenotype of circulating NK and T cells of 27 MM patients before and after treatment with an anti-CTLA-4 antibody (tremelimumab). These immune cell profiles were compared to healthy controls. The RNA expression data of the MM biopsies indicated the presence of NK cells in a subgroup of patients. We demonstrated that NK cells recognize MM cell lines and that IL-15 stimulation improved NK cell-mediated lysis in vitro. Using multivariate projection models, we found that MM patients had a perturbed ratio of CD56
Substances chimiques
Antibodies, Monoclonal, Humanized
0
Antineoplastic Agents
0
CD56 Antigen
0
CTLA-4 Antigen
0
Cytokines
0
tremelimumab
QEN1X95CIX
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2238-2248Informations de copyright
© 2019 UICC.
Références
Robinson BW, Musk AW, Lake RA. Malignant mesothelioma. Lancet 2005;366:397-408.
Lin RT, Takahashi K, Karjalainen A, et al. Ecological association between asbestos-related diseases and historical asbestos consumption: an international analysis. Lancet 2007;369:844-9.
Odgerel CO, Takahashi K, Sorahan T, et al. Estimation of the global burden of mesothelioma deaths from incomplete national mortality data. Occup Environ Med 2017;74:851-8.
Baas P, Fennell D, Kerr KM, et al. Malignant pleural mesothelioma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 2015;26(Suppl 5):v31-9.
Taioli E, Wolf AS, Camacho-Rivera M, et al. Determinants of survival in malignant pleural mesothelioma: a surveillance, epidemiology, and end results (SEER) study of 14,228 patients. PLoS One 2015;10:e0145039.
Zalcman G, Mazieres J, Margery J, et al. Bevacizumab for newly diagnosed pleural mesothelioma in the mesothelioma Avastin Cisplatin Pemetrexed study (MAPS): a randomised, controlled, open-label, phase 3 trial. Lancet 2016;387:1405-14.
Aerts JG, Hegmans JP. Tumor-specific cytotoxic T cells are crucial for efficacy of immunomodulatory antibodies in patients with lung cancer. Cancer Res 2013;73:2381-8.
Moretta A. Natural killer cells and dendritic cells: rendezvous in abused tissues. Nat Rev Immunol 2002;2:957-64.
Hegmans JP, Aerts JG. Immunomodulation in cancer. Curr Opin Pharmacol 2014;17:17-21.
Karre K, Ljunggren HG, Piontek G, et al. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 1986;319:675-8.
Kiessling R, Klein E, Pross H, et al. “natural” killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur J Immunol 1975;5:117-21.
Malmberg KJ, Carlsten M, Bjorklund A, et al. Natural killer cell-mediated immunosurveillance of human cancer. Semin Immunol 2017;31:20-9.
Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
Drake CG, Jaffee E, Pardoll DM. Mechanisms of immune evasion by tumors. Adv Immunol 2006;90:51-81.
Topalian SL, Drake CG, Pardoll DM. Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell 2015;27:450-61.
Bueno R, Stawiski EW, Goldstein LD, et al. Comprehensive genomic analysis of malignant pleural mesothelioma identifies recurrent mutations, gene fusions and splicing alterations. Nat Genet 2016;48:407-16.
Hegmans JP, Hemmes A, Hammad H, et al. Mesothelioma environment comprises cytokines and T-regulatory cells that suppress immune responses. Eur Respir J 2006;27:1086-95.
Dozier J, Zheng H, Adusumilli PS. Immunotherapy for malignant pleural mesothelioma: current status and future directions. Transl Lung Cancer Res 2017;6:315-24.
Thomas A, Hassan R. Immunotherapies for non-small-cell lung cancer and mesothelioma. Lancet Oncol 2012;13:e301-10.
Calabro L, Morra A, Fonsatti E, et al. Tremelimumab for patients with chemotherapy-resistant advanced malignant mesothelioma: an open-label, single-arm, phase 2 trial. Lancet Oncol 2013;14:1104-11.
Calabro L, Morra A, Fonsatti E, et al. Efficacy and safety of an intensified schedule of tremelimumab for chemotherapy-resistant malignant mesothelioma: an open-label, single-arm, phase 2 study. Lancet Respir Med 2015;3:301-9.
Addeo A, Buffoni L, Di Maio M. Is there room for second-line treatment of pleural malignant mesothelioma? JAMA Oncol 2017;3:1170-1.
Maio M, Scherpereel A, Calabro L, et al. Tremelimumab as second-line or third-line treatment in relapsed malignant mesothelioma (DETERMINE): a multicentre, international, randomised, double-blind, placebo-controlled phase 2b trial. Lancet Oncol 2017;18:1261-73.
Byrne MJ, Nowak AK. Modified RECIST criteria for assessment of response in malignant pleural mesothelioma. Ann Oncol 2004;15:257-60.
Ramachandran H, Laux J, Moldovan I, et al. Optimal thawing of cryopreserved peripheral blood mononuclear cells for use in high-throughput human immune monitoring studies. Cell 2012;1:313-24.
Mutti L, Valle MT, Balbi B, et al. Primary human mesothelioma cells express class II MHC, ICAM-1 and B7-2 and can present recall antigens to autologous blood lymphocytes. Int J Cancer 1998;78:740-9.
Orengo AM, Spoletini L, Procopio A, et al. Establishment of four new mesothelioma cell lines: characterization by ultrastructural and immunophenotypic analysis. Eur Respir J 1999;13:527-34.
Dutta M, Subramani E, Taunk K, et al. Investigation of serum proteome alterations in human endometriosis. J Proteomics 2015;114:182-96.
Tallerico R, Cristiani CM, Staaf E, et al. IL-15, TIM-3 and NK cells subsets predict responsiveness to anti-CTLA-4 treatment in melanoma patients. Oncoimmunology 2017;6:e1261242.
Conlon KC, Lugli E, Welles HC, et al. Redistribution, hyperproliferation, activation of natural killer cells and CD8 T cells, and cytokine production during first-in-human clinical trial of recombinant human interleukin-15 in patients with cancer. J Clin Oncol 2015;33:74-82.
Nowak AK, Lesterhuis WJ, Hughes BGM, et al. DREAM: a phase II study of durvalumab with first line chemotherapy in mesothelioma-first results. J Clin Oncol 2018;36:8503-3.
de Coana YP, Wolodarski M, Poschke I, et al. Ipilimumab treatment decreases monocytic MDSCs and increases CD8 effector memory T cells in long-term survivors with advanced melanoma. Oncotarget 2017;8:21539-53.
Barry KC, Hsu J, Broz ML, et al. A natural killer-dendritic cell axis defines checkpoint therapy-responsive tumor microenvironments. Nat Med 2018;24:1178-91.
Manning LS, Bowman RV, Darby SB, et al. Lysis of human malignant mesothelioma cells by natural killer (NK) and lymphokine-activated killer (LAK) cells. Am Rev Respir Dis 1989;139:1369-74.
Pahl J, Cerwenka A. Tricking the balance: NK cells in anti-cancer immunity. Immunobiology 2017;222:11-20.
Meloni F, Morosini M, Solari N, et al. Foxp3 expressing CD4+ CD25+ and CD8+CD28− T regulatory cells in the peripheral blood of patients with lung cancer and pleural mesothelioma. Hum Immunol 2006;67:1-12.
Han S, Feng S, Xu L, et al. Tim-3 on peripheral CD4(+) and CD8(+) T cells is involved in the development of glioma. DNA Cell Biol 2014;33:245-50.
Jiang J, Jin MS, Kong F, et al. Decreased galectin-9 and increased Tim-3 expression are related to poor prognosis in gastric cancer. PLoS One 2013;8:e81799.
Marcq E, Waele J, Audenaerde JV, et al. Abundant expression of TIM-3, LAG-3, PD-1 and PD-L1 as immunotherapy checkpoint targets in effusions of mesothelioma patients. Oncotarget 2017;8:89722-35.
Gueugnon F, Leclercq S, Blanquart C, et al. Identification of novel markers for the diagnosis of malignant pleural mesothelioma. Am J Pathol 2011;178:1033-42.
Wang W, Guo H, Geng J, et al. Tumor-released Galectin-3, a soluble inhibitory ligand of human NKp30, plays an important role in tumor escape from NK cell attack. J Biol Chem 2014;289:33311-9.
Pasero C, Gravis G, Granjeaud S, et al. Highly effective NK cells are associated with good prognosis in patients with metastatic prostate cancer. Oncotarget 2015;6:14360-73.
Storojeva I, Boulay JL, Ballabeni P, et al. Prognostic and predictive relevance of DNAM-1, SOCS6 and CADH-7 genes on chromosome 18q in colorectal cancer. Oncology 2005;68:246-55.
Koch J, Steinle A, Watzl C, et al. Activating natural cytotoxicity receptors of natural killer cells in cancer and infection. Trends Immunol 2013;34:182-91.
Glasner A, Ghadially H, Gur C, et al. Recognition and prevention of tumor metastasis by the NK receptor NKp46/NCR1. J Immunol 2012;188:2509-15.
Mirjacic Martinovic KM, Babovic N, Dzodic RR, et al. Decreased expression of NKG2D, NKp46, DNAM-1 receptors, and intracellular perforin and STAT-1 effector molecules in NK cells and their dim and bright subsets in metastatic melanoma patients. Melanoma Res 2014;24:295-304.
Romano E, Kusio-Kobialka M, Foukas PG, et al. Ipilimumab-dependent cell-mediated cytotoxicity of regulatory T cells ex vivo by nonclassical monocytes in melanoma patients. Proc Natl Acad Sci USA 2015;112:6140-5.
Khan S, Burt DJ, Ralph C, et al. Tremelimumab (anti-CTLA4) mediates immune responses mainly by direct activation of T effector cells rather than by affecting T regulatory cells. Clin Immunol 2011;138:85-96.