Control of Plasmodium falciparum erythrocytic cycle: γδ T cells target the red blood cell-invasive merozoites

Blood

Volumn 118, Issue 26, 2011, Pages 6952-6962

  Giulia, Costa ^a,b   Loizon, Séverine ^a,b   Guenot, Marianne ^a,b   Mocan, Iulia ^a,b   Halary, Franck ^a,b   De Saint Basile, Geneviève ^c   Pitard, Vincent ^a,b   Chanet Merville, Julie Dé ^a,b   Moreau, Jean François ^a,b,d   Troye Blomberg, Marita ^e   Mercereau Puijalon, Odile ^a   Behr, Charlotte ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c INSERM   (France)

^d BORDEAUX UNIVERSITY HOSPITAL   (France)

^e STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULYSIN; PERFORIN;

ARTICLE; DEGRANULATION; ERYTHROCYTE; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; MALARIA FALCIPARUM; MEROZOITE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; SCHIZONT; T LYMPHOCYTE ACTIVATION; V GAMMA 9V DELTA 2 T LYMPHOCYTE;

EID: 84255160942     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-08-376111     Document Type: Article

References (49)

1. Cohen S, Mc GI, Carrington S. gamma-Globulin and acquired immunity to human malaria. Nature. 1961;192:733-737.
2. Sabchareon A, Burnouf T, Ouattara D, et al. Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. Am J Trop Med Hyg. 1991;45(3):297-308.
3. Stevenson MM, Riley EM. Innate immunity to malaria. Nat Rev Immunol. 2004;4(3):169-180. (Pubitemid 38339083)
4. Moser B, Eberl M. gammadelta T cells: novel initiators of adaptive immunity. Immunol Rev. 2007;215:89-102. (Pubitemid 46212232)
5. Morita CT, Jin C, Sarikonda G, Wang H. Nonpeptide antigens, presentation mechanisms, and immunological memory of human Vgamma2Vdelta2 T cells: discriminating friend from foe through the recognition of prenyl pyrophosphate antigens. Immunol Rev. 2007;215:59-76. (Pubitemid 46212230)
6. Behr C, Poupot R, Peyrat MA, et al. Plasmodium falciparum stimuli for human gammadelta T cells are related to phosphorylated antigens of mycobacteria. Infect Immun. 1996;64(8):2892-2896. (Pubitemid 26256121)
7. Eberl M, Hintz M, Reichenberg A, Kollas AK, Wiesner J, Jomaa H. Microbial isoprenoid biosynthesis and human gammadelta T cell activation. FEBS Lett. 2003;544(1-3):4-10. (Pubitemid 36628027)
8. Roussilhon C, Agrapart M, Ballet JJ, Bensussan A. T lymphocytes bearing the gamma delta T cell receptor in patients with acute Plasmodium falciparum malaria. J Infect Dis. 1990;162(1):283-285. (Pubitemid 20223998)
9. Ho M, Tongtawe P, Kriangkum J, et al. Polyclonal expansion of peripheral gamma delta T cells in human Plasmodium falciparum malaria. Infect Immun. 1994;62(3):855-862. (Pubitemid 24065565)
10. Elloso MM, van der Heyde HC, vande Waa JA, Manning DD, Weidanz WP. Inhibition of Plasmodium falciparum in vitro by human gamma delta T cells. J Immunol. 1994;153(3):1187-1194. (Pubitemid 24228510)
11. Troye-Blomberg M, Worku S, Tangteerawatana P, et al. Human gamma delta T cells that inhibit the in vitro growth of the asexual blood stages of the Plasmodium falciparum parasite express cytolytic and proinflammatory molecules. Scand J Immunol. 1999;50(6):642-650.
12. Trager W, Jensen JB. Human malaria parasites in continuous culture. Science. 1976;193(4254):673-675.
13. Pasvol G, Wilson RJ, Smalley ME, Brown J. Separation of viable schizont-infected red cells of Plasmodium falciparum from human blood. Ann Trop Med Parasitol. 1978;72(1):87-88. (Pubitemid 9112070)
14. Salmon BL, Oksman A, Goldberg DE. Malaria parasite exit from the host erythrocyte: a twostep process requiring extraerythrocytic proteolysis. Proc Natl Acad Sci U S A. 2001;98(1):271-276. (Pubitemid 32095899)
15. Halary F, Pitard V, Dlubek D, et al. Shared reactivity of V{delta}2(neg) {gamma}{delta} T cells against cytomegalovirus-infected cells and tumor intestinal epithelial cells. J Exp Med. 2005;201(10):1567-1578. (Pubitemid 40721002)
16. Stepp SE, Dufourcq-Lagelouse R, Le Deist F, et al. Perforin gene defects in familial hemophagocytic lymphohistiocytosis. Science. 1999;286(5446):1957- 1959. (Pubitemid 129515904)
17. Bonneville M, Moreau JF, Blokland E, et al. T lymphocyte cloning from rejected human kidney allograft. Recognition repertoire of alloreactive T cell clones. J Immunol. 1988;141(12):4187-4195. (Pubitemid 19018204)
18. Zheng CF, Ma LL, Jones GJ, et al. Cytotoxic CD4+ T cells use granulysin to kill Cryptococcus neoformans, and activation of this pathway is defective in HIV patients. Blood. 2007;109(5):2049-2057. (Pubitemid 46348205)
19. Sena-Esteves M, Tebbets JC, Steffens S, Crombleholme T, Flake AW. Optimized largescale production of high titer lentivirus vector pseudotypes. J Virol Methods. 2004;122(2):131-139. (Pubitemid 39470183)
20. Betts MR, Brenchley JM, Price DA, et al. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods. 2003;281(1-2):65-78. (Pubitemid 37324571)
21. van der Heyde HC, Elloso MM, vande Waa J, Schell K, Weidanz WP. Use of hydroethidine and flow cytometry to assess the effects of leukocytes on the malarial parasite Plasmodium falciparum. Clin Diagn Lab Immunol. 1995;2(4):417-425.
22. Chung WH, Hung SI, Yang JY, et al. Granulysin is a key mediator for disseminated keratinocyte death in Stevens-Johnson syndrome and toxic epidermal necrolysis. Nat Med. 2008;14(12):1343-1350.
23. Caccamo N, Meraviglia S, Ferlazzo V, et al. Differential requirements for antigen or homeostatic cytokines for proliferation and differentiation of human Vgamma9Vdelta2 naive, memory and effector T cell subsets. Eur J Immunol. 2005;35(6):1764-1772. (Pubitemid 40862324)
24. Elloso MM,Wallace M, Manning DD,Weidanz WP. The effects of interleukin-15 on human gammadelta T cell responses to Plasmodium falciparum in vitro. Immunol Lett. 1998;64(2-3):125-132. (Pubitemid 28553022)
25. D'Ombrain MC, Hansen DS, Simpson KM, Schofield L. gammadelta-T cells expressing NK receptors predominate over NK cells and conventional T cells in the innate IFN-gamma response to Plasmodium falciparum malaria. Eur J Immunol. 2007;37(7):1864-1873. (Pubitemid 47065125)
26. Farouk SE, Mincheva-Nilsson L, Krensky AM, Dieli F, Troye-Blomberg M. Gamma delta T cells inhibit in vitro growth of the asexual blood stages of Plasmodium falciparum by a granule exocytosis- dependent cytotoxic pathway that requires granulysin. Eur J Immunol. 2004;34(8):2248-2256. (Pubitemid 39256106)
27. Barry M, Bleackley RC. Cytotoxic T lymphocytes: all roads lead to death. Nat Rev Immunol. 2002;2(6):401-409. (Pubitemid 37328747)
28. Stenger S, Hanson DA, Teitelbaum R, et al. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science. 1998;282(5386):121-125. (Pubitemid 28471143)
29. Dieli F, Troye-Blomberg M, Ivanyi J, et al. Granulysin- dependent killing of intracellular and extracellular Mycobacterium tuberculosis by Vgamma9/Vdelta2 T lymphocytes. J Infect Dis. 2001;184(8):1082-1085. (Pubitemid 32955129)
30. Walch M, Latinovic-Golic S, Velic A, et al. Perforin enhances the granulysin-induced lysis of Listeria innocua in human dendritic cells. BMC Immunol. 2007;8:14.
31. Lang F, Peyrat MA, Constant P, et al. Early activation of human V gamma 9V delta 2 T cell broad cytotoxicity and TNF production by nonpeptidic mycobacterial ligands. J Immunol. 1995;154(11):5986-5994.
32. Dieli F, Poccia F, Lipp M, et al. Differentiation of effector/memory Vdelta2 T cells and migratory routes in lymph nodes or inflammatory sites. J Exp Med. 2003;198(3):391-397. (Pubitemid 36980610)
33. Ralph SA, van Dooren GG, Waller RF, et al. Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol. 2004;2(3):203-216. (Pubitemid 39490083)
34. Behr C, Dubois P. Preferential expansion of V gamma 9 V delta 2 T cells following stimulation of peripheral blood lymphocytes with extracts of Plasmodium falciparum. Int Immunol. 1992;4(3):361-366.
35. Goerlich R, Hacker G, Pfeffer K, Heeg K, Wagner H. Plasmodium falciparum merozoites primarily stimulate the V gamma 9 subset of human gamma/delta T cells. Eur J Immunol. 1991;21(10):2613-2616.
36. Waterfall M, Black A, Riley E. Gammadelta+ T cells preferentially respond to live rather than killed malaria parasites. Infect Immun. 1998;66(5):2393-2398. (Pubitemid 28194152)
37. Peña SV, Hanson DA, Carr BA, Goralski TJ, Krensky AM. Processing, subcellular localization, and function of 519 (granulysin), a human late T cell activation molecule with homology to small, lytic, granule proteins. J Immunol. 1997;158(6):2680-2688. (Pubitemid 127470525)
38. Pipkin ME, Lieberman J. Delivering the kiss of death: progress on understanding how perforin works. Curr Opin Immunol. 2007;19(3):301-308. (Pubitemid 46687016)
39. Ernst WA, Thoma-Uszynski S, Teitelbaum R, et al. Granulysin, a T cell product, kills bacteria by altering membrane permeability. J Immunol. 2000;165(12):7102-7108. (Pubitemid 32001185)
40. Li Q, Dong C, Deng A, et al. Hemolysis of erythrocytes by granulysin-derived peptides but not by granulysin. Antimicrob Agents Chemother. 2005;49(1):388-397. (Pubitemid 40065816)
41. Krensky AM, Clayberger C. Granulysin: a novel host defense molecule. Am J Transplant. 2005;5(8):1789-1792. (Pubitemid 41039850)
42. Garcia CR, de Azevedo MF, Wunderlich G, Budu A, Young JA, Bannister L. Plasmodium in the postgenomic era: new insights into the molecular cell biology of malaria parasites. Int Rev Cell Mol Biol. 2008;266:85-156.
43. Nitcheu J, Bonduelle O, Combadiere C, et al. Perforin-dependent brain-infiltrating cytotoxic CD8+ T lymphocytes mediate experimental cerebral malaria pathogenesis. J Immunol. 2003;170(4):2221-2228. (Pubitemid 36197447)
44. Ochoa MT, Stenger S, Sieling PA, et al. T-cell release of granulysin contributes to host defense in leprosy. Nat Med. 2001;7(2):174-179. (Pubitemid 32148483)
45. Roiko MS, Carruthers VB. New roles for perforins and proteases in apicomplexan egress. Cell Microbiol. 2009;11(10):1444-1452.
46. Bordessoule D, Gaulard P, Mason DY. Preferential localisation of human lymphocytes bearing gamma delta T cell receptors to the red pulp of the spleen. J Clin Pathol. 1990;43(6):461-464. (Pubitemid 20173179)
47. Safeukui I, Correas JM, Brousse V, et al. Retention of Plasmodium falciparum ring-infected erythrocytes in the slow, open microcirculation of the human spleen. Blood. 2008;112(6):2520-2528.
48. Deng A, Chen S, Li Q, Lyu SC, Clayberger C, Krensky AM. Granulysin, a cytolytic molecule, is also a chemoattractant and proinflammatory activator. J Immunol. 2005;174(9):5243-5248. (Pubitemid 40593162)
49. Wilhelm M, Kunzmann V, Eckstein S, et al. gamma delta T cells for immune therapy of patients with lymphoid malignancies. Blood. 2003;102:200-206. (Pubitemid 36759655)