Dynamic Alteration in HLA-E Expression and Soluble HLA-E via Interaction with Natural Killer Cells in Gastric Cancer.
Journal
Annals of surgical oncology
ISSN: 1534-4681
Titre abrégé: Ann Surg Oncol
Pays: United States
ID NLM: 9420840
Informations de publication
Date de publication:
Feb 2023
Feb 2023
Historique:
received:
03
05
2022
accepted:
18
08
2022
pubmed:
24
9
2022
medline:
6
1
2023
entrez:
23
9
2022
Statut:
ppublish
Résumé
Some reports showed the immune tolerance of soluble human leukocyte antigen E (HLA-E), but the role that soluble HLA-E plays in gastric cancer (GC) is unknown. We aimed to clarify the molecular mechanism and clinical significance of soluble HLA-E in GC. We examined the expression of HLA-E on GC cells and soluble HLA-E under co-culture with natural killer (NK) cells in a time-dependent manner. Changes in NK cell activity were investigated using anti-NK group 2 member A (NKG2A) antibodies in the presence of soluble HLA-E. Expression of soluble HLA-E in the serum of GC patients was determined. Whereas HLA-E expression on GC cells peaked with interferon (IFN)-γ secretion by NK cells in a time-dependent manner, soluble HLA-E was upregulated in conditioned medium. Pre-incubation with anti-NKG2A antibodies increased the activation of NKG2A HLA-E expression dynamically changes on GC cells and in conditioned medium. Furthermore, soluble HLA-E can contribute to immune escape in GC cell lines, which may have significance in clinical practice. Moreover, soluble HLA-E may be a potential prognostic biomarker.
Sections du résumé
BACKGROUND
BACKGROUND
Some reports showed the immune tolerance of soluble human leukocyte antigen E (HLA-E), but the role that soluble HLA-E plays in gastric cancer (GC) is unknown. We aimed to clarify the molecular mechanism and clinical significance of soluble HLA-E in GC.
METHODS
METHODS
We examined the expression of HLA-E on GC cells and soluble HLA-E under co-culture with natural killer (NK) cells in a time-dependent manner. Changes in NK cell activity were investigated using anti-NK group 2 member A (NKG2A) antibodies in the presence of soluble HLA-E. Expression of soluble HLA-E in the serum of GC patients was determined.
RESULTS
RESULTS
Whereas HLA-E expression on GC cells peaked with interferon (IFN)-γ secretion by NK cells in a time-dependent manner, soluble HLA-E was upregulated in conditioned medium. Pre-incubation with anti-NKG2A antibodies increased the activation of NKG2A
CONCLUSIONS
CONCLUSIONS
HLA-E expression dynamically changes on GC cells and in conditioned medium. Furthermore, soluble HLA-E can contribute to immune escape in GC cell lines, which may have significance in clinical practice. Moreover, soluble HLA-E may be a potential prognostic biomarker.
Identifiants
pubmed: 36149610
doi: 10.1245/s10434-022-12505-0
pii: 10.1245/s10434-022-12505-0
doi:
Substances chimiques
Culture Media, Conditioned
0
Histocompatibility Antigens Class I
0
HLA Antigens
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1240-1252Informations de copyright
© 2022. Society of Surgical Oncology.
Références
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424.
doi: 10.3322/caac.21492
Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252–64.
doi: 10.1038/nrc3239
Kang YK, Boku N, Satoh T, et al. Nivolumab in patients with advanced gastric or gastro-oesophageal junction cancer refractory to, or intolerant of, at least two previous chemotherapy regimens (ONO-4538-12, ATTRACTION-2): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet. 2017;390(10111):2461–71.
doi: 10.1016/S0140-6736(17)31827-5
Creelan BC, Antonia SJ. The NKG2A immune checkpoint—a new direction in cancer immunotherapy. Nat Rev Clin Oncol. 2019;16(5):277–8.
doi: 10.1038/s41571-019-0182-8
Borst L, van der Burg SH, van Hall T. The NKG2A-HLA-E axis as a novel checkpoint in the tumor microenvironment. Clin Cancer Res. 2020;26(21):5549–56.
doi: 10.1158/1078-0432.CCR-19-2095
Mingari MC, Pietra G, Moretta L. Immune checkpoint inhibitors: anti-NKG2A antibodies on board. Trends Immunol. 2019;40(2):83–5.
doi: 10.1016/j.it.2018.12.009
Zhang C, Liu Y. Targeting NK cell checkpoint receptors or molecules for cancer immunotherapy. Front Immunol. 2020;11:1295.
doi: 10.3389/fimmu.2020.01295
Rodgers JR, Cook RG. MHC class Ib molecules bridge innate and acquired immunity. Nat Rev Immunol. 2005;5(6):459–71.
doi: 10.1038/nri1635
André P, Denis C, Soulas C, et al. Anti-NKG2A mAb Is a checkpoint inhibitor that promotes anti-tumor immunity by unleashing both T and NK cells. Cell. 2018;175(7):1731-1743.e13.
doi: 10.1016/j.cell.2018.10.014
van Montfoort N, Borst L, Korrer MJ, et al. NKG2A blockade potentiates CD8 T cell immunity induced by cancer vaccines. Cell. 2018;175(7):1744-1755.e15.
doi: 10.1016/j.cell.2018.10.028
Spaans VM, Peters AA, Fleuren GJ, Jordanova ES. HLA-E expression in cervical adenocarcinomas: association with improved long-term survival. J Transl Med. 2012;10:184.
doi: 10.1186/1479-5876-10-184
Hiraoka N, Ino Y, Hori S, et al. Expression of classical human leukocyte antigen class I antigens, HLA-E and HLA-G, is adversely prognostic in pancreatic cancer patients. Cancer Sci. 2020;111(8):3057–70.
doi: 10.1111/cas.14514
Ishigami S, Arigami T, Okumura H, et al. Human leukocyte antigen (HLA)-E and HLA-F expression in gastric cancer. Anticancer Res. 2015;35(4):2279–85.
Morinaga T, Iwatsuki M, Yamashita K, et al. Evaluation of HLA-E expression combined with natural killer cell status as a prognostic factor for advanced gastric cancer. Ann Surg Oncol. 2022;29(8):4951–60.
doi: 10.1245/s10434-022-11665-3
Cichocki F, Miller JS. Setting traps for NKG2A gives NK cell immunotherapy a fighting chance. J Clin Invest. 2019;129(5):1839–41.
doi: 10.1172/JCI128480
Malmberg KJ, Levitsky V, Norell H, et al. IFN-gamma protects short-term ovarian carcinoma cell lines from CTL lysis via a CD94/NKG2A-dependent mechanism. J Clin Invest. 2002;110(10):1515–23.
doi: 10.1172/JCI0215564
Derré L, Corvaisier M, Charreau B, et al. Expression and release of HLA-E by melanoma cells and melanocytes: potential impact on the response of cytotoxic effector cells. J Immunol. 2006;177(5):3100–7.
doi: 10.4049/jimmunol.177.5.3100
Coupel S, Moreau A, Hamidou M, Horejsi V, Soulillou JP, Charreau B. Expression and release of soluble HLA-E is an immunoregulatory feature of endothelial cell activation. Blood. 2007;109(7):2806–14.
doi: 10.1182/blood-2006-06-030213
Wagner B, da Silva Nardi F, Schramm S, et al. HLA-E allelic genotype correlates with HLA-E plasma levels and predicts early progression in chronic lymphocytic leukemia. Cancer. 2017;123(5):814–23.
doi: 10.1002/cncr.30427
Shou ZX, Jin X, Zhao ZS. Upregulated expression of ADAM17 is a prognostic marker for patients with gastric cancer. Ann Surg. 2012;256(6):1014–22.
doi: 10.1097/SLA.0b013e3182592f56
Yamashita K, Iwatsuki M, Yasuda-Yoshihara N, et al. Trastuzumab upregulates programmed death ligand-1 expression through interaction with NK cells in gastric cancer. Br J Cancer. 2021;124(3):595–603.
doi: 10.1038/s41416-020-01138-3
Kamiya T, Seow SV, Wong D, Robinson M, Campana D. Blocking expression of inhibitory receptor NKG2A overcomes tumor resistance to NK cells. J Clin Invest. 2019;129(5):2094–106.
doi: 10.1172/JCI123955
Orme JJ, Jazieh KA, Xie T, et al. ADAM10 and ADAM17 cleave PD-L1 to mediate PD-(L)1 inhibitor resistance. Oncoimmunology. 2020;9(1):1744980.
doi: 10.1080/2162402X.2020.1744980
Lo Monaco E, Tremante E, Cerboni C, et al. Human leukocyte antigen E contributes to protect tumor cells from lysis by natural killer cells. Neoplasia. 2011;13(9):822–30.
doi: 10.1593/neo.101684
Allard M, Oger R, Vignard V, et al. Serum soluble HLA-E in melanoma: a new potential immune-related marker in cancer. PLoS One. 2011;6(6):e21118.
doi: 10.1371/journal.pone.0021118
Goel R, Kabeerdoss J, Mohan H, et al. Soluble-HLA-E: a follow up biomarker in Takayasu arteritis, independent of HLA-E genotype. Int J Rheum Dis. 2018;21(2):532–40.
doi: 10.1111/1756-185X.13027