Plasmodium falciparum-infected erythrocytes induce granzyme b by NK cells through expression of host-Hsp70

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Böttger, Evelyn ^a   Multhoff, Gabriele ^b,c   Kun, Jürgen F J ^a   Esen, Meral ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD94 ANTIGEN; GRANZYME B; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 70 TKD PEPTIDE; HLA E ANTIGEN; IMMUNOSTIMULATING AGENT; LIPOCORTIN 5; MICA B PROTEIN; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2C; PERFORIN; PROTEIN; UNCLASSIFIED DRUG; GRANZYME; KLRC2 PROTEIN, HUMAN; KLRD1 PROTEIN, HUMAN; MESSENGER RNA; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY C; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY D;

APOPTOSIS; ARTICLE; CELL CONTACT; CELL STIMULATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; ENZYME RELEASE; ERYPTOSIS; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; FLOW CYTOMETRY; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; PARASITE DEVELOPMENT; PLASMODIUM FALCIPARUM; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAINING; TARGET CELL DESTRUCTION; UPREGULATION; WESTERN BLOTTING; BIOLOGICAL MODEL; BIOSYNTHESIS; BLOOD; CELL COMMUNICATION; CELL LINE; COCULTURE; ERYTHROCYTE LIFESPAN; GENETICS; GROWTH, DEVELOPMENT AND AGING; HELA CELL; IMMUNOLOGY; IN VITRO STUDY; INNATE IMMUNITY; METABOLISM; NATURAL KILLER CELL; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY;

PLASMODIUM FALCIPARUM;

APOPTOSIS; CELL COMMUNICATION; CELL LINE; COCULTURE TECHNIQUES; ERYTHROCYTE AGING; ERYTHROCYTES; GRANZYMES; HELA CELLS; HOST-PARASITE INTERACTIONS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; IMMUNITY, INNATE; KILLER CELLS, NATURAL; MODELS, IMMUNOLOGICAL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY D; PLASMODIUM FALCIPARUM; RNA, MESSENGER;

EID: 84858211907     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033774     Document Type: Article

References (41)

1. Horowitz A, Newman KC, Evans JH, Korbel DS, Davis DM, et al. (2010) Cross-talk between T cells and NK cells generates rapid effector responses to Plasmodium falciparum-infected erythrocytes. J Immunol 184: 6043-52.
2. Newman KC, Korbel DS, Hafalla JC, Riley EM, (2006) Cross-talk with myeloid accessory cells regulates human natural killer cell interferon-gamma responses to malaria. PLoS Pathog 2: e118.
3. Degli-Esposti MA, Smyth MJ, (2005) Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat Rev Immunol 5: 112-114.
4. Lucas M, Schachterle W, Oberle K, Aichele P, Diefenbach A, (2007) Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 26: 503-517.
5. Kiessling R, Klein E, Wigzell H, (1975) "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 2: 112-117.
6. Herberman RB, Nunn ME, Holden HT, Lavrin DH, (1975) Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors. II. Characterization of effector cells. Int J Cancer 16: 230-239.
7. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, et al. (2001) Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol 19: 197-223.
8. Elsner L, Flugge PF, Lozano J, Muppala V, Eiz-Vesper B, et al. (2010) The endogenous danger signals HSP70 and MICA cooperate in the activation of cytotoxic effector functions of NK cells. J Cell Mol Med 14: 992-1002.
9. Ljunggren HG, Karre K, (1990) In search of the 'missing self': MHC molecules and NK cell recognition. Immunol Today 11: 237-244.
10. Korbel DS, Newman KC, Almeida CR, Davis DM, Riley EM, (2005) Heterogeneous human NK cell responses to Plasmodium falciparum-infected erythrocytes. J Immunol 175: 7466-7473.
11. Artavanis-Tsakonas K, Riley EM, (2002) Innate immune response to malaria: rapid induction of IFN-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes. J Immunol 169: 2956-2963.
12. Artavanis-Tsakonas K, Eleme K, McQueen KL, Cheng NW, Parham P, et al. (2003) Activation of a subset of human NK cells upon contact with Plasmodium falciparum-infected erythrocytes. J Immunol 171: 5396-5405.
13. Banumathy G, Singh V, Tatu U, (2002) Host chaperones are recruited in membrane-bound complexes by Plasmodium falciparum. J Biol Chem 277: 3902-3912.
14. Multhoff G, (2009) Activation of natural killer cells by heat shock protein 70. 2002. Int J Hyperthermia 25: 169-175.
15. Multhoff G, (2009) Hyperthermia classic commentary: Activation of natural killer (NK) cells by heat shock protein 70, Gabriele Multhoff, International Journal of Hyperthermia, 2002;18:576-585. Int J Hyperthermia 25: 176-179.
16. Stangl S, Wortmann A, Guertler U, Multhoff G, (2006) Control of metastasized pancreatic carcinomas in SCID/beige mice with human IL-2/TKD-activated NK cells. J Immunol 176: 6270-6276.
17. Joly AL, Wettstein G, Mignot G, Ghiringhelli F, Garrido C, (2010) Dual role of heat shock proteins as regulators of apoptosis and innate immunity. J Innate Immun 2: 238-247.
18. Matzinger P, (1998) An innate sense of danger. Semin Immunol 10: 399-415.
19. Multhoff G, Pfister K, Gehrmann M, Hantschel M, Gross C, et al. (2001) A 14-mer Hsp70 peptide stimulates natural killer (NK) cell activity. Cell Stress Chaperones 6: 337-344.
20. Gross C, Koelch W, DeMaio A, Arispe N, Multhoff G, (2003) Cell surface-bound heat shock protein 70 (Hsp70) mediates perforin-independent apoptosis by specific binding and uptake of granzyme B. J Biol Chem 278: 41173-41181.
21. de Carvalho EG, Böttger E, Hoang VT, Kremsner PG, Kun JF, (2011) Limited response of NK92 cells to Plasmodium falciparum-infected erythrocytes. Malar J 10: 311.
22. de Koning-Ward TF, Gilson PR, Boddey JA, Rug M, Smith BJ, et al. (2009) A newly discovered protein export machine in malaria parasites. Nature 459: 945-950.
23. Marti M, Good RT, Rug M, Knuepfer E, Cowman AF, (2004) Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306: 1930-1933.
24. Haldar K, Mohandas N, (2007) Erythrocyte remodeling by malaria parasites. Curr Opin Hematol 14: 203-209.
25. Giribaldi G, Ulliers D, Mannu F, Arese P, Turrini F, (2001) Growth of Plasmodium falciparum induces stage-dependent haemichrome formation, oxidative aggregation of band 3, membrane deposition of complement and antibodies, and phagocytosis of parasitized erythrocyte. Br J Haematol 113: 492-499.
26. Stangl S, Gross C, Pockley AG, Asea AA, Multhoff G, (2008) Influence of Hsp70 and HLA-E on the killing of leukemic blasts by cytokine/Hsp70 peptide-activated human natural killer (NK) cells. Cell Stress Chaperones 13: 221-230.
27. Gross C, Schmidt-Wolf IG, Nagaraj S, Gastpar R, Ellwart J, et al. (2003) Heat shock protein 70-reactivity is associated with increased cell surface density of CD94/CD56 on primary natural killer cells. Cell Stress Chaperones 8: 348-360.
28. Grossman WJ, Verbsky JW, Tollefsen BL, Kemper C, Atkinson JP, et al. (2004) Differential expression of granzymes A and B in human cytotoxic lymphocyte subsets and T regulatory cells. Blood 104: 2840-2848.
29. Bratke K, Kuepper M, Bade B, Virchow JC Jr, Luttmann W, (2005) Differential expression of human granzymes A, B, and K in natural killer cells and during CD8+ T cell differentiation in peripheral blood. Eur J Immunol 35: 2608-2616.
30. Fehniger TA, Cai SF, Cao X, Bredemeyer AJ, Presti RM, et al. (2007) Acquisition of murine NK cell cytotoxicity requires the translation of a pre-existing pool of granzyme B and perforin mRNAs. Immunity 26: 798-811.
31. Kim TD, Lee SU, Yun S, Sun HN, Lee SH, et al. (2011) Human microRNA-27a* targets Prf1 and GzmB expression to regulate NK-cell cytotoxicity. Blood 118: 5476-86.
32. Hermssen CC, Konijnenberg Y, Mulder L, Loé C, van Deuren M, et al. (2003) Circulating concentrations of soluble granzyme A and B increase during natural and experimental Plasmodium falciparum infections. Clin Exp Immunol 132: 467-472.
33. Lang F, Gulbins E, Lerche H, Huber SM, Kempe DS, et al. (2008) Eryptosis, a window to systemic disease. Cell Physiol Biochem 22: 373-380.
34. Föller M, Bobbala D, Koka S, Huber SM, Gulbins E, et al. (2009) Suicide for survival-death of infected erythrocytes as a host mechanism to survive malaria. Cell Physiol Biochem 24: 133-140.
35. Krause SW, Gastpar R, Andreesen R, Gross C, Ulrich H, et al. (2004) Treatment of Colon and Lung Cancer Patients with ex Vivo Heat Shock Protein 70-Peptide-Activated, Autologous Natural Killer Cells: A Clinical Phase I Trial. Clin Cancer Res 10: 3699-3707.
36. Binder RJ, (2008) Heat-shock protein-based vaccines for cancer and infectious disease. Expert Rev Vaccines 7: 383-393.
37. Calderwood D, (2005) Message in a bottle: role of 70-kDa heat shock protein family in anti-tumor immunity. Eur J Imm 35: 2518-27.
38. Sun JC, Lopez-Verges S, Kim CC, DeRisi JL, Lanier LL, (2011) NK cells and immune "memory". J Immunol 186: 1891-1897.
39. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, et al. (2011) Innate or adaptive immunity? The example of natural killer cells. Science 331: 44-49.
40. Trager W, Jensen JB, (1976) Human malaria parasites in continuous culture. J Parasitol 91: 484-486.
41. Föller M, Braun M, Quadri SM, Lang E, Mahmud H, et al. (2010) Temperature sensitvity of suicidal erythrocyte death. Eur J Clin Invest 40: 534-40.