Journal of Shanghai Jiao Tong University (Medical Science) >

2021 , Vol. 41 >Issue 5: 659 - 664

DOI: https://doi.org/10.3969/j.issn.1674-8115.2021.05.017

Review

Mechanisms related to regulation of natural killer cell activity by exosomes derived from malignant tumor cells

  • Ting-wei LU ,
  • Jian-jun ZHANG ,
  • Wan-tao CHEN
Expand
  • Department of Oral and Maxillofacial-Head & Neck Oncology, Shanghai Ninth People's Hospital, College of Stomatology, Shanghai Jiao Tong University School of Medicine; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology & Shanghai Research Institute of Stomatology, Shanghai 200011, China

Online published: 2021-05-27

Supported by

National Natural Science Foundation of China(81874126);Project of Science?and?Technology?Commission?of?Shanghai?Municipality(18JC1413700);Innovation Research Team of High-Level Local Universities in Shanghai(SSMU-ZLCX20180502)

Fold

Abstract

Exosomes are a kind of extracellular vesicles that play the role of transmitting information among cells. Through transporting of substances to regulate the physiological and pathological functions of various cells, it can affect the progress of malignant tumors. Natural killer (NK) cell is an indispensable part of the human immune system, and is important in the development of cancers. In the tumor microenvironment, tumor-derived exosomes (TDEXs) can act on NK cells, adjusting their functions, and modifying the interaction between NK cells and other immune cells, resulting in the change of the immune response. In recent years, the research on the relationship between NK cells and tumor exosomes has become a hot topic. The effects of TDEXs from different cancers on the activities of NK cells are summarized in this paper.

Key words： malignant tumor; tumor-derived exosome; natural killer cell; activity

Cite this article

Ting-wei LU , Jian-jun ZHANG , Wan-tao CHEN . Mechanisms related to regulation of natural killer cell activity by exosomes derived from malignant tumor cells[J]. Journal of Shanghai Jiao Tong University (Medical Science), 2021 , 41(5) : 659 -664 . DOI: 10.3969/j.issn.1674-8115.2021.05.017

References

1 Johnstone RM, Adam M, Hammond JR, et al. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes)[J]. J Biol Chem, 1987, 262(19): 9412-9420.
2 Melo SA, Luecke LB, Kahlert C, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer[J]. Nature, 2015, 523(7559): 177-182.
3 Niu Y, Zhang C, Sun Z, et al. PtdIns(4)P regulates retromer-motor interaction to facilitate dynein-cargo dissociation at the trans-Golgi network[J]. Nat Cell Biol, 2013, 15(4): 417-429.
4 Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends[J]. J Cell Biol, 2013, 200(4): 373-383.
5 Xiao C, Song F, Zheng YL, et al. Exosomes in head and neck squamous cell carcinoma[J]. Front Oncol, 2019, 9: 894.
6 Schulz M, Salamero-Boix A, Niesel K, et al. Microenvironmental regulation of tumor progression and therapeutic response in brain metastasis[J]. Front Immunol, 2019, 10: 1713.
7 Liu YF, Gu Y, Cao XT. The exosomes in tumor immunity[J]. Oncoimmunology, 2015, 4(9): e1027472.
8 Banik D, Moufarrij S, Villagra A. Immunoepigenetics combination therapies: an overview of the role of HDACs in cancer immunotherapy[J]. Int J Mol Sci, 2019, 20(9): 2241.
9 Zorrilla SR, García AG, Carrión AB, et al. Exosomes in head and neck cancer. Updating and revisiting[J]. J Enzym Inhib Med Chem, 2019, 34(1): 1641-1651.
10 Matsumoto A, Takahashi Y, Nishikawa M, et al. Accelerated growth of B16BL6 tumor in mice through efficient uptake of their own exosomes by B16BL6 cells[J]. Cancer Sci, 2017, 108(9): 1803-1810.
11 Ye LS, Zhang Q, Cheng YS, et al. Tumor-derived exosomal HMGB1 fosters hepatocellular carcinoma immune evasion by promoting TIM-1+ regulatory B cell expansion[J]. J Immunother Cancer, 2018, 6(1): 1-15.
12 Yang C, Shen CY, Feng T, et al. Noncoding RNA in NK cells[J]. J Leukoc Biol, 2019, 105(1): 63-71.
13 Sun YY, Guo MF, Feng YJ, et al. Effect of ginseng polysaccharides on NK cell cytotoxicity in immunosuppressed mice[J]. Exp Ther Med, 2016, 12(6): 3773-3777.
14 Han QJ, Zhao HJ, Jiang Y, et al. HCC-derived exosomes: critical player and target for cancer immune escape[J]. Cells, 2019, 8(6): 558.
15 Sakaue T, Koga H, Iwamoto H, et al. Glycosylation of ascites-derived exosomal CD133: a potential prognostic biomarker in patients with advanced pancreatic cancer[J]. Med Mol Morphol, 2019, 52(4): 198-208.
16 高斌, 熊莹晖, 黄泽炳, 等. 乙肝相关性肝细胞癌患者血清外泌体miR-1290水平的变化及其诊断价值[J]. 中国普通外科杂志, 2019, 28(1): 31-38.
17 Shi R, Wang PY, Li XY, et al. Exosomal levels of miRNA-21 from cerebrospinal fluids associated with poor prognosis and tumor recurrence of glioma patients[J]. Oncotarget, 2015, 6(29): 26971-26981.
18 Ying X, Wu QF, Wu XL, et al. Epithelial ovarian cancer-secreted exosomal miR-222-3p induces polarization of tumor-associated macrophages[J]. Oncotarget, 2016, 7(28): 43076-43087.
19 Chen G, Huang AC, Zhang W, et al. Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response[J]. Nature, 2018, 560(7718): 382-386.
20 Lundholm M, Schr?der M, Nagaeva O, et al. Prostate tumor-derived exosomes down-regulate NKG2D expression on natural killer cells and CD8+ T cells: mechanism of immune evasion[J]. PLoS One, 2014, 9(9): e108925.
21 Chow A, Zhou WY, Liu L, et al. Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-κB[J]. Sci Rep, 2014, 4: 5750.
22 Zhang T, Lemoi BA, Sentman CL. Chimeric NK-receptor-bearing T cells mediate antitumor immunotherapy[J]. Blood, 2005, 106(5): 1544-1551.
23 Schmiedel D, Tai J, Yamin R, et al. The RNA binding protein IMP3 facilitates tumor immune escape by downregulating the stress-induced ligands ULPB2 and MICB[J]. Elife, 2016,16(5). DOI: 10.7554/eLife.13426.
24 Guerra N, Tan YX, Joncker NT, et al. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy[J]. Immunity, 2008, 28(4): 571-580.
25 Ludwig S, Floros T, Theodoraki MN, et al. Suppression of lymphocyte functions by plasma exosomes correlates with disease activity in patients with head and neck cancer[J]. Clin Cancer Res, 2017, 23(16): 4843-4854.
26 Labani-Motlagh A, Israelsson P, Ottander U, et al. Differential expression of ligands for NKG2D and DNAM-1 receptors by epithelial ovarian cancer-derived exosomes and its influence on NK cell cytotoxicity[J]. Tumor Biol, 2016, 37(4): 5455-5466.
27 Alipoor SD, Mortaz E, Varahram M, et al. The potential biomarkers and immunological effects of tumor-derived exosomes in lung cancer[J]. Front Immunol, 2018, 9: 819.
28 Zhang Y, Lazaro AM, Lavingia B, et al. Typing for all known MICA alleles by group-specific PCR and SSOP[J]. Hum Immunol, 2001, 62(6): 620-631.
29 Ashiru O, Boutet P, Fernández-Messina L, et al. Natural killer cell cytotoxicity is suppressed by exposure to the human NKG2D ligand MICA*008 that is shed by tumor cells in exosomes[J]. Cancer Res, 2010, 70(2): 481-489.
30 Lafontaine L, Chaudhry P, Lafleur MJ, et al. Transforming growth factor β regulates proliferation and invasion of rat placental cell lines[J]. Biol Reprod, 2011, 84(3): 553-559.
31 Chandran PA, Keller A, Weinmann L, et al. The TGF-β-inducible miR-23a cluster attenuates IFN-γ levels and antigen-specific cytotoxicity in human CD8+ T cells[J]. J Leukoc Biol, 2014, 96(4): 633-645.
32 Sharma P, Ludwig S, Muller L, et al. Immunoaffinity-based isolation of melanoma cell-derived exosomes from plasma of patients with melanoma[J]. J Extracell Vesicles, 2018, 7(1): 1435138.
33 Szczepanski MJ, Szajnik M, Welsh A, et al. Blast-derived microvesicles in sera from patients with acute myeloid leukemia suppress natural killer cell function via membrane-associated transforming growth factor-β1[J]. Haematologica, 2011, 96(9): 1302-1309.
34 Yamada N, Tsujimura N, Kumazaki M, et al. Colorectal cancer cell-derived microvesicles containing microRNA-1246 promote angiogenesis by activating Smad 1/5/8 signaling elicited by PML down-regulation in endothelial cells[J]. Biochim et Biophys Acta, 2014, 1839(11): 1256-1272.
35 Berchem G, Noman MZ, Bosseler M, et al. Hypoxic tumor-derived microvesicles negatively regulate NK cell function by a mechanism involving TGF-β and miR23a transfer[J]. OncoImmunology, 2016, 5(4): e1062968.
36 Filipazzi P, Bürdek M, Villa A, et al. Recent advances on the role of tumor exosomes in immunosuppression and disease progression[J]. Semin Cancer Biol, 2012, 22(4): 342-349.
37 Whiteside TL. Immune modulation of T-cell and NK (natural killer) cell activities by TEXs (tumour-derived exosomes)[J]. Biochem Soc Trans, 2013, 41(1): 245-251.
38 Liu BD, Sun LJ, Liu Q, et al. A cytoplasmic NF-κB interacting long noncoding RNA blocks IκB phosphorylation and suppresses breast cancer metastasis[J]. Cancer Cell, 2015, 27(3): 370-381.
39 Chatterjee S, Burns TF. Targeting heat shock proteins in cancer: a promising therapeutic approach[J]. Int J Mol Sci, 2017, 18(9): 1978.
40 Elsner L, Muppala V, Gehrmann M, et al. The heat shock protein HSP70 promotes mouse NK cell activity against tumors that express inducible NKG2D ligands[J]. J Immunol, 2007, 179(8): 5523-5533.
41 Gastpar R, Gehrmann M, Bausero MA, et al. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells[J]. Cancer Res, 2005, 65(12): 5238-5247.
42 Vulpis E, Cecere F, Molfetta R, et al. Genotoxic stress modulates the release of exosomes from multiple myeloma cells capable of activating NK cell cytokine production: role of HSP70/TLR2/NF-κB axis[J]. Oncoimmunology, 2017, 6(3): e1279372.
43 Fujita F, Taniguchi Y, Kato T, et al. Identification of NAP1, a regulatory subunit of IκB kinase-related kinases that potentiates NF-κB signaling[J]. Mol Cell Biol, 2003, 23(21): 7780-7793.
44 Wang YN, Qin X, Zhu XQ, et al. Oral cancer-derived exosomal NAP1 enhances cytotoxicity of natural killer cells via the IRF-3 pathway[J]. Oral Oncol, 2018, 76: 34-41.
45 Kandasamy M, Suryawanshi A, Tundup S, et al. RIG-I signaling is critical for efficient polyfunctional T cell responses during influenza virus infection[J]. PLoS Pathog, 2016, 12(7): e1005754.
46 Schuldner M, D?rsam B, Shatnyeva O, et al. Exosome-dependent immune surveillance at the metastatic niche requires BAG6 and CBP/p300-dependent acetylation of p53[J]. Theranostics, 2019, 9(21): 6047-6062.
47 Da?ler-Plenker J, Reiners KS, van den Boorn JG, et al. RIG-I activation induces the release of extracellular vesicles with antitumor activity[J]. OncoImmunology, 2016, 5(10): e1219827.
48 Zwirner NW, Domaica CI. Cytokine regulation of natural killer cell effector functions[J]. Biofactors, 2010, 36(4): 274-288.
49 Imai C, Iwamoto S, Campana D. Genetic modification of primary natural killer cells overcomes inhibitory signals and induces specific killing of leukemic cells[J]. Blood, 2005, 106(1): 376-383.
50 Li Q, Huang QP, Huyan T, et al. Bifacial effects of engineering tumour cell-derived exosomes on human natural killer cells[J]. Exp Cell Res, 2018, 363(2): 141-150.
51 van Audenaerde JRM, de Waele J, Marcq E, et al. Interleukin-15 stimulates natural killer cell-mediated killing of both human pancreatic cancer and stellate cells[J]. Oncotarget, 2017, 8(34): 56968-56979.
52 Ohno SI, Takanashi M, Sudo K, et al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells[J]. Mol Ther, 2013, 21(1): 185-191.
53 Xie YF, Bai O, Zhang HF, et al. Membrane-bound HSP70-engineered myeloma cell-derived exosomes stimulate more efficient CD8+ CTL- and NK-mediated antitumour immunity than exosomes released from heat-shocked tumour cells expressing cytoplasmic HSP70[J]. J Cell Mol Med, 2010, 14(11): 2655-2666.
54 Yang NB, Li SS, Li GX, et al. The role of extracellular vesicles in mediating progression, metastasis and potential treatment of hepatocellular carcinoma[J]. Oncotarget, 2017, 8(2): 3683-3695.
55 Borrelli C, Ricci B, Vulpis E, et al. Drug-induced senescent multiple myeloma cells elicit NK cell proliferation by direct or exosome-mediated IL15 trans-presentation[J]. Cancer Immunol Res, 2018, 6(7): 860-869.
56 Koyama Y, Ito T, Hasegawa A, et al. Exosomes derived from tumor cells genetically modified to express Mycobacterium tuberculosis antigen: a novel vaccine for cancer therapy[J]. Biotechnol Lett, 2016, 38(11): 1857-1866.
57 Xie CQ, Ji N, Tang ZG, et al. The role of extracellular vesicles from different origin in the microenvironment of head and neck cancers[J]. Mol Cancer, 2019, 18(1): 1-15.
58 Ma T, Chen YQ, Chen YH, et al. MicroRNA-132, delivered by mesenchymal stem cell-derived exosomes, promote angiogenesis in myocardial infarction[J]. Stem Cells Int, 2018, 2018: 3290372.
Options
Outlines

/

〈 〉