Differential expression of ligands for NKG2D and DNAM-1 receptors by epithelial ovarian cancer-derived exosomes and its influence on NK cell cytotoxicity

Tumor Biology

Volumn 37, Issue 4, 2016, Pages 5455-5466

  Labani Motlagh, Alireza ^a   Israelsson, Pernilla ^a   Ottander, Ulrika ^a   Lundin, Eva ^a   Nagaev, Ivan ^a   Nagaeva, Olga ^a   Dehlin, Eva ^a   Baranov, Vladimir ^a   Mincheva Nilsson, Lucia ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

Cytotoxicity; DNAM 1 CD266; Epithelial ovarian cancer EOC; Exosomes; MICA B; Nectin 2; NKG2D; PVR; Tumor; ULBP

Indexed keywords

NATURAL KILLER CELL RECEPTOR NKG2D; PROTEIN DNAM 1; RECEPTOR; UNCLASSIFIED DRUG; CD226 ANTIGEN; KLRK1 PROTEIN, HUMAN; LIGAND; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K; T LYMPHOCYTE ANTIGEN;

ARTICLE; ASCITES FLUID; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; DEGRANULATION; DOWN REGULATION; EXOSOME; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; OVARY CARCINOMA; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; K-562 CELL LINE; METABOLISM; MONONUCLEAR CELL; NEOPLASM; OVARY TUMOR; PATHOLOGY; SIGNAL TRANSDUCTION;

ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; EXOSOMES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; K562 CELLS; KILLER CELLS, NATURAL; LEUKOCYTES, MONONUCLEAR; LIGANDS; NEOPLASMS, GLANDULAR AND EPITHELIAL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; OVARIAN NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 84946924480     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-015-4313-2     Document Type: Article

References (32)

1. Campbell KS, Hasegawa J. Natural killer cell biology: an update and future direction. J Allergy Clin Immunol. 2013;132:536–44.
2. Lanier LL. NK cell recognition. Annu Rev Immunol. 2005;23:225–74.
3. Smyth MJ, Swann J, Cretney E, Zerafa N, Yokoyama WM, Hayakawa Y. NKG2D function protects the host from tumor initiation. J Exp Med. 2005;202:583–8.
4. Guerra N, Tan YX, Jincker NT, Choy A, Gallardo F, Xiong N, et al. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity. 2008;28:571–80.
5. El-Sherbiny YM, Meade JL, Holmes TD, McConagle D, Mackie SL, Morgan AW, et al. The requirement for DNAM-1, NKG2D and NKp46 in the natural killer cell-mediated killing of myeloma cells. Cancer Res. 2007;67:8444–9.
6. Raulet DH. Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol. 2003;3:781–90.
7. Hildreth JE, Gotch FM, Hildreth PD, McMichael AJ. A human lymphocyte associated antigen involved in cell-mediated lympholysis. Eur J Immunol. 1983;13:202–8.
8. Gahmberg CG. Leukocyte adhesion: CD11/CD18 integrins and intercellular adhesion molecules. Curr Opin Cell Biol. 1997;9:643–50.
9. Fuchs A, Colonna M. The role of NK cell recognition of nectin and nectin-like proteins in tumor surveillance. Semin Cancer Biol. 2006;16:359–66.
10. Carlsten M, Björkström N, Norell H, Bryceson Y, van Hall T, Baumann B, et al. DNAX accessory molecule-1 mediated recognition of freshly isolated ovarian carcinoma by resting natural killer cells. Cancer Res. 2007;67:1317–25.
11. Gubbels JA, Claussen N, Kapur AK, Connor JP, Patankar MS. The detection, treatment, and biology of epithelial ovarian cancer. J Ovarian Res. 2010;3:8.
12. Yigit R, Massuger LF, Figdor CG, Torensma R. Ovarian cancer creates a suppressive microenvironment to escape immune elimination. Gynecol Oncol. 2010;117:366–72.
13. Holschneider CH, Berek JS. Ovarian cancer: epidemiology, biology, and prognostic factors. Semin Surg Oncol. 2000;19(1):3–10.
14. Mincheva-Nilsson L, Baranov V. Cancer exosomes and NKG2D receptor-ligand interactions: impairing NKG2D-mediated cytotoxicity and anti-tumor immune surveillance. Semin Cancer Biol. 2014;28:24–30.
15. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009;55:611–22.
16. Stenqvist AC, Nagaeva O, Baranov V, Mincheva-Nilsson L. Exosomes secreted by human placenta carry functional Fas ligand and TRAIL molecules and convey apoptosis in activated immune cells, suggesting exosome-mediated immune privilege of the fetus. J Immunol. 2013;191:5515–23.
17. Mincheva-Nilsson L, Nagaeva O, Chen T, Stendahl U, Antsiferova J, Mogren I, et al. Placenta-derived soluble MHC class I chain-related molecules down-regulate NKG2D receptor on peripheral blood mononuclear cells during human pregnancy: a possible novel immune escape mechanism for fetal survival. J Immunol. 2006;176:3585–92.
18. Hedlund M, Stenqvist AC, Nagaeva O, Kjellberg L, Wulff M, Baranov V, et al. Human placenta expresses and secretes NKG2D ligands via exosomes that down-modulate the cognate receptor expression: evidence for immunosuppressive function. J Immunol. 2009;183:340–51.
19. Greening DW, Xu R, Ji H, Tauro BJ, Simpson RJ. A protocol for exosome isolation and characterization: evaluation of ultracentrifugation, density-gradient separation and immunoaffinity capture methods. In Proteomic profiling: Methods and Protocols. Anton Posh (ed). Methods in molecular Biology, vol. 1295, DOI 10.1007/978-1-4939-2550-6_15, 2015.
20. Kiessling R, Klein E, Wigzell H. Natural killer cells in the mouse.I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur J Immunol. 1975;5:112–7.
21. Costello RT, Fauriat C, Sivori S, Marcenaro E, Olive D. NK cells: innate immunity against hematological malignancies. Trends Immunol. 2004;25:328–33.
22. Lanier LL. A renaissance for the tumor immunosurveillance hypothesis. Nat Med. 2001;7:1178–80.
23. Kaplan-Lefko PJ, Chen TM, Ittmann MM, Barrios RJ, Ayala GE, Huss WJ, et al. Pathobiology of autochthonous prostate cancer in a pre-clinical transgenic mouse model. Prostate. 2003;55:219–37.
24. Groh V, Reinhard R, Secrist H, Grabstein KH, Spies T. Broad tumor-associated expression and recognition by tumor-derived gamma-delta T cells of MICA and MICB. Proc Natl Acad Sci U S A. 1999;96:6879–84.
25. Clayton A, Mitchell JP, Court J, Linnane S, Mason MD, Tabi Z. Human tumor-derived exosomes downmodulate NKG2D expression. J Immunol. 2008;180:7249–58.
26. Lundholm L, Schroder M, Nagaeva O, Baranov V, Widmark A, Mincheva-Nilsson L, et al. Prostate tumor-derived exosomes down-regulate NKG2D expression on natural killer cells and CD8+ T cells: mechanism of immune evasion. PLoS ONE. 2014;9:e108925.
27. Clayton A, Mason MD. Exosomes in tumor immunity. Curr Oncol. 2009;16:46–9.
28. Hedlund M, Nagaeva O, Kargl D, Baranov V, Mincheva-Nilsson L. Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells. PLoS One. 2011;6:e16899.
29. Mizuki N, Ota M, Kimura M, Ohno S, Ando H, Katsuyama Y, et al. Triplet repeat polymorphism in the transmembrane region of MICA gene: a strong association of six CGT repetitions with Becet disease. Proc Natl Acad Sci U S A. 1997;94:1298–303.
30. Ashiru O, Boutet P, Fernandez-Messina L, Agüera-González S, Skepper J, Valés-Gómez M, et al. Natural killer cell cytotoxicity is suppressed by exposure to the human NKG2D ligand MICA*0008 that is shed by tumor cells in exosomes. Cancer Res. 2010;70:481–9.
31. Ghaderi M, Hjelmstrom, Hallmans G, Wiklund F, Lenner P, Dillner J, et al. MICA gene polymorphism and the risk to develop cervical epithelial neoplasia. Hum Immunol. 1999;60:970–3.
32. Filipazzi P, Bürdek M, Villa A, Rivoltini L, Huber V. Recent advances on the role of tumor exosomes in immunosuppression and disease progression. Semin Cancer Biol. 2012;22:342–9.