Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Hedlund, Malin ^a   Nagaeva, Olga ^a   Kargl, Dominic ^a   Baranov, Vladimir ^a   Mincheva Nilsson, Lucia ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NATURAL KILLER CELL RECEPTOR NKG2D; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; HLA ANTIGEN CLASS 1; HYDROGEN PEROXIDE; KLRK1 PROTEIN, HUMAN; LIGAND; MHC CLASS I RELATED CHAIN A; MHC CLASS I-RELATED CHAIN A; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K; SIGNAL PEPTIDE; ULBP1 PROTEIN, HUMAN; ULBP2 PROTEIN, HUMAN;

ARTICLE; B CELL LEUKEMIA; B CELL LYMPHOMA; CELL SPECIFICITY; CONTROLLED STUDY; ENDOSOME; EXOSOME; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; LEUKEMIA CELL LINE; LYMPHOCYTE FUNCTION; LYMPHOMA CELL LINE; MOLECULAR SIZE; NATURAL KILLER CELL; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN SECRETION; T CELL LEUKEMIA; T CELL LYMPHOMA; TEMPERATURE STRESS; UPREGULATION; DRUG EFFECT; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOMA; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SECRETION; TEMPERATURE; TUMOR CELL CULTURE;

EXOSOMES; GPI-LINKED PROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; HYDROGEN PEROXIDE; IMMUNE TOLERANCE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JURKAT CELLS; LEUKEMIA, B-CELL; LEUKEMIA, T-CELL; LIGANDS; LYMPHOMA; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; OXIDATIVE STRESS; STRESS, PHYSIOLOGICAL; TEMPERATURE; TUMOR CELLS, CULTURED;

EID: 79952159254     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016899     Document Type: Article

References (36)

1. Raulet DH, Guerra N, (2009) Oncogenic stress sensed by the immune system: role of natural killer cell receptors. Nature Rev Immunol 9: 568-578.
2. Guerra N, Tan YX, Joncker NT, Choy A, Gallardo F, et al. (2008) NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 28: 571-580.
3. Coudert JD, Held W, (2006) The role of NKG2D receptor in tumor immunity. Sem Cancer Biol 16: 333-343.
4. Pende D, Cantoni C, Rivera P, Vitale M, Castriconi R, et al. (2001) Role of NKG2D in tumor cell lysis mediated by human NK cells: cooperation with natural cytotoxicity receptors and capability of recognizing tumors of neoepithelial origin. Eur J Immunol 31: 1076-1086.
5. Cerwenka A, Baron JL, Lanier LL, (2001) Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer -mediated rejection of a MHC class I-bearing tumor in vivo. Proc Natl Acad Sci USA 98: 11521-11526.
6. Jamieson AM, Diefenbach A, McMahon CW, Xiong N, Carlyle JR, et al. (2002) The role of NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 17: 19-29.
7. Hayashi T, Imai K, Morishita Y, Hayashi I, Kusunoki Y, et al. (2006) Identification of the NKG2D haplotypes associated with natural cytotoxic activity of peripheral blood lymphocytes and cancer immunosurveillance. Cancer Res 66: 563-570.
8. Champsaur M, Lanier LL, (2010) Effect of NKG2D ligand expression on host immune response. Immunol Rev 235: 267-285.
9. Salih HR, Holdenrieder S, Steinle A, (2008) Soluble NKG2D ligands: prevalence, release, and functional impact. Front in Biosci 13: 3448-3456.
10. Gonzales C, Groh V, Spies T, (2006) Immunobiology of human NKG2D and its ligands. Curr Top Microbiol Immunol 298: 121-138.
11. Salih HR, Rammensee HG, Steinle A, (2002) Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J Immunol 169: 4098-4102.
12. Clayton A, Tabi Z, (2005) Exosomes and the MICA-NKG2D system in cancer. Blood Cells Mol Dis 34: 206-213.
13. Clayton A, Mitchel JP, Court J, Linnane S, Mason MD, et al. (2008) Human tumor-derived exosomes down-modulate NKG2D expression. J Immunol 180: 7249-7258.
14. Mincheva-Nilsson L, Nagaeva O, Chen T, Stendahl U, Antsiferova J, et al. (2006) Placenta-derived soluble MHC class I chain-related molecules down-regulate NKG2D receptor on peripheral mononuclear cells during human pregnancy: a possible novel immune escape mechanism for fetal survival. J Immunol 176: 3585-3592.
15. Hedlund M, Stenqvist AC, Nagaeva O, Kjellberg L, Wulff M, et al. (2009) Human placenta expresses and secretes NKG2D ligands via exosomes that down-modulate the cognate receptor expression: evidence for immunosuppressive function. J Immunol 183: 340-351.
16. van Niel G, Porto-Carreiro I, Simoes S, Raposo G, (2006) Exosomes: a common pathway for a specialized function. J Biochem 140: 13-21.
17. Skog J, Würdinger T, van Rijn S, Meijer DH, Cainche L, et al. (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumor growth and provide diagnostic biomarkers. Nat Cell Biol 10: 1470-1476.
18. Nilsson J, Skog J, Nordstrand A, Baranov V, Mincheva-Nilsson L, et al. (2009) Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer. Br J Cancer 100: 1603-1607.
19. Viaud S, Thery C, Plox S, Turzs T, Lapierre V, et al. (2010) Dendritic cell-derived exosomes for cancer immunotherapy: What is next? Cancer res 70: 1281-1285.
20. Clayton A, Nason MD, (2009) Exosomes in tumor immunity. Curr Oncol 16: 46-49.
21. Wodnar-Filipowicz A, Kalberer CP, (2006) Function of natural killer cells in immune defence against human leukaemia. Swiss MedWkly 136: 359-364.
22. Clayton A, Turkes A, Navabi H, Mason MD, Tabi Z, (2005) Induction of heat shock proteins in B-cell exosomes. J Cell Sci 118: 3631-3638.
23. Lehmann BD, Paine MS, Brooks AM, McCubrey JA, Renegar RH, et al. (2008) Senescence-associated exosome release from human prostate cancer cells. Cancer Res 68: 7864-7871.
24. Nückel H, Switala M, Sellmann L, Horn PA, Dürig J, et al. (2010) The prognostic significance of soluble NKG2D ligands in B-cell chronic leukemia. Leukemia 24: 1152-1159.
25. Lanca T, Correia DV, Moita CF, Raquel H, Neves-Costa A, et al. (2010) The MHC class I protein ULBP1 is a nonredundant determinant of leukemia/lymphoma susceptibility to gamma delta T-cell cytotoxicity. Blood 115: 2407-2411.
26. Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, et al. (2001) Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat med 7: 297-303.
27. Andre F, Schartz NE, Movassagh M, Flament C, Pautier P, et al. (2002) Malignant effusions and immunological tumor-derived exosomes. Lancet 360: 295-305.
28. Clayton A, Mitchell JP, Court J, Mason MD, Tabi Z, (2007) Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2. Cancer Res 67: 7458-7466.
29. Taylor D, Gercel-Taylor C, (2005) Tumor-derived exosomes and their role in cancer associated T-cell signalling defects. Br J Cancer 92: 305-311.
30. Mincheva-Nilsson L, Baranov V, (2010) The role of placental exosomes in reproduction. Am J Reprod Immunol 63: 520-33.
31. Groh V, Wu J, Yee C, Spies T, (2002) Tumor-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419: 734-738.
32. Salih HR, Antropius H, Gieseke F, Lutz SZ, Kantz L, et al. (2003) Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukaemia. Blood 102: 1389-1396.
33. O'Reilly LA, Tai L, Lee L, Kruse EA, Grabow S, et al. (2009) Membrane-bound Fas ligand only is essential for Fas-induced apoptosis. Nature 461: 659-663.
34. Abusamra A, Zhong Z, Zheng X, Li M, Ichim T, et al. (2005) Tumor exosomes expressing Fas ligand mediate CD8+ T-cell apoptosis. Blood Cells Mol Dis 35: 169-173.
35. Fernandez-Messina L, Ashiru O, Boutet O, Agäuera-Gonzales S, Skepper JN, et al. (2010) Differential mechanisms of shedding of the glycosylphosphatidylinositol (GPI)-anchored NKG2D ligands. J Biol Chem 285: 8543-8551.
36. Koga T, Harada H, Shi TS, Okada S, Suico MA, et al. (2005) Hyperthermia suppresses the cytotoxicity of NK cells via down-regulation of perforin/granzyme B expression. Biochem Biophys Res Commun 337: 1319-1323.