(E)-4-Hydroxy-3-methyl-but-2 enyl pyrophosphate-stimulated Vγ9Vδ2 T cells possess T helper type 1-promoting adjuvant activity for human monocyte-derived dendritic cells

Cancer Immunology, Immunotherapy

Volumn 59, Issue 7, 2010, Pages 1109-1120

  Dunne, Margaret R ^a,b   Madrigal Estebas, Laura ^b   Tobin, Laura M ^b   Doherty, Derek G ^a,b  

^a ST JAMES S HOSPITAL   (Ireland)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Cytokines; Dendritic cells; Human; Immunotherapy; V 9V 2 T cells

Indexed keywords

4 HYDROXY 3 METHYL BUT 2 ENYL PYROPHOSPHATE; CD40 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; CYTOKINE; DENDRITIC CELL VACCINE; GLYCOPROTEIN P 15095; HLA DR ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; PYROPHOSPHORIC ACID DERIVATIVE; UNCLASSIFIED DRUG; 4 HYDROXY 3 METHYLBUT 2 ENYL PYROPHOSPHATE; 4-HYDROXY-3-METHYLBUT-2-ENYL PYROPHOSPHATE; LYMPHOCYTE ANTIGEN RECEPTOR; PYROPHOSPHATE;

ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOLYSIS; EFFECTOR CELL; HELPER CELL; HUMAN; HUMAN CELL; MEMORY T LYMPHOCYTE; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VGAMMA9 VDELTA9 T LYMPHOCYTE; CELL CULTURE; CYTOLOGY; DENDRITIC CELL; DRUG EFFECT; FLOW CYTOMETRY; IMMUNOLOGY; METABOLISM; TH1 CELL;

ANTIGEN-PRESENTING CELLS; ANTIGENS, CD11C; ANTIGENS, CD86; CELL DIFFERENTIATION; CELLS, CULTURED; DENDRITIC CELLS; DIPHOSPHATES; FLOW CYTOMETRY; HLA-DR ANTIGENS; HUMANS; INTERLEUKIN-10; INTERLEUKIN-12; MONOCYTES; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTES; TH1 CELLS;

EID: 77953080449     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-010-0839-8     Document Type: Article

References (48)

1. CT Morita C Jin G Sarikonda H Wang 2007 Nonpeptide antigens, presentation mechanisms, and immunological memory of human Vγ9Vδ2 T cells: discriminating friend from foe through the recognition of prenyl pyrophosphate antigens Immunol Rev 215 59 76 10.1111/j.1600-065X.2006.00479.x 1:CAS:528:DC%2BD2sXjsVKrtro%3D 17291279 (Pubitemid 46212230)
2. B Moser M Eberl 2007 γδ T cells: novel initiators of adaptive immunity Immunol Rev 215 89 102 10.1111/j.1600-065X.2006.00472.x 1:CAS:528:DC%2BD2sXjsVKrtrg%3D 17291281 (Pubitemid 46212232)
3. T Hara Y Mizuno K Takaki H Takada H Akeda T Aoki M Nagata K Ueda G Matsuzaki Y Yoshikai 1992 Predominant activation and expansion of Vγ9-bearing γδ T cells in vivo as well as in vitro in Salmonella infection J Clin Invest 90 204 210 10.1172/JCI115837 1:CAS:528:DyaK38XltV2rtb4%3D 1386086
4. F Dieli M Troye-Blomberg J Ivanyi JJ Fournié AM Krensky M Bonneville MA Peyrat N Caccamo G Sireci A Salerno 2001 Granulysin-dependent killing of intracellular and extracellular Mycobacterium tuberculosis by Vγ9Vδ2 T lymphocytes J Infect Dis 184 1082 1085 10.1086/323600 1:CAS:528:DC%2BD3MXotVWnsb8%3D 11574927 (Pubitemid 32955129)
5. P Wrobel H Shojaei B Schittek F Gieseler B Wollenberg H Kalthoff D Kabelitz D Wesch 2007 Lysis of a broad range of epithelial tumor cells by human γδ T cells: involvement of NKG2D ligands and T-cell receptor-versus NKG2D-dependent recognition Scand J Immunol 66 320 328 10.1111/j.1365-3083.2007. 01963.x 1:CAS:528:DC%2BD2sXpvVGqt70%3D 17635809 (Pubitemid 47063194)
6. C Agrati E Cimini A Sacchi V Bordoni C Gioia R Casetti F Turchi M Tripodi F Martini 2009 Activated Vγ9Vδ2 T cells trigger granulocyte functions via MCP-2 release J Immunol 182 522 529 1:CAS:528:DC%2BD1cXhsFCisLzN 19109184
7. M Eberl GW Roberts S Meuter JD Williams N Topley B Moser 2009 A rapid crosstalk of human γδ T cells and monocytes drives the acute inflammation in bacterial infections PLoS Pathog 5 e1000308 10.1371/journal. ppat.1000308 19229322
8. J Ismaili V Olislagers R Poupot JJ Fournié M Goldman 2002 Human γδ T cells induce dendritic cell maturation Clin Immunol 103 296 302 10.1006/clim.2002.5218 1:CAS:528:DC%2BD38Xls1Oisr4%3D 12173304 (Pubitemid 34666753)
9. L Conti R Casetti M Cardone B Varano A Martino F Belardelli F Poccia S Gessani 2005 Reciprocal activating interaction between dendritic cells and pamidronate-stimulated γδ T cells: role of CD86 and inflammatory cytokines J Immunol 174 252 260 1:CAS:528:DC%2BD2cXhtFaiurrM 15611247
10. MC Devilder S Maillet I Bouyge-Moreau E Donnadieu M Bonneville E Scotet 2006 Potentiation of antigen-stimulated Vγ9Vδ2 T cell cytokine production by immature dendritic cells (DC) and reciprocal effect on DC maturation J Immunol 176 1386 1393 1:CAS:528:DC%2BD28XlsFyiuw%3D%3D 16424165 (Pubitemid 43134280)
11. N Caccamo L Battistini M Bonneville F Poccia JJ Fournié S Meraviglia G Borsellino RA Kroczek C La Mendola E Scotet F Dieli A Salerno 2006 CXCR5 identifies a subset of Vγ9Vδ2 T cells which secrete IL-4 and IL-10 and help B cells for antibody production J Immunol 177 5290 5295 1:CAS:528:DC%2BD28XhtVansrnO 17015714
12. M Brandes K Willimann B Moser 2005 Professional antigen-presentation function by human γδ T Cells Science 309 264 268 10.1126/science.1110267 1:CAS:528:DC%2BD2MXlsl2jtLg%3D 15933162 (Pubitemid 40967855)
13. + αβ T cell responses Proc Natl Acad Sci USA 106 2307 2312 10.1073/pnas.0810059106 1:CAS:528: DC%2BD1MXit1yksrk%3D 19171897
14. Y Tanaka S Sano E Nieves G De Libero D Rosa RL Modlin MB Brenner BR Bloom CT Morita 1994 Nonpeptide ligands for human γδ T cells Proc Natl Acad Sci USA 91 8175 8179 10.1073/pnas.91.17.8175 1:CAS:528:DyaK2cXlsFGitrY%3D 8058775 (Pubitemid 24253909)
15. Y Tanaka CT Morita Y Tanaka E Nieves MB Brenner BR Bloom 1995 Natural and synthetic non-peptide antigens recognized by human γδ T cells Nature 375 155 158 10.1038/375155a0 1:CAS:528:DyaK2MXls1Wisrk%3D 7753173
16. M Hintz A Reichenberg B Altincicek U Bahr RM Gschwind AK Kollas E Beck J Wiesner M Eberl H Jomaa 2001 Identification of (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate as a major activator for human γδ T cells in Escherichia coli FEBS Lett 509 317 322 10.1016/S0014-5793(01)03191-X 1:CAS:528:DC%2BD3MXovF2hs7w%3D 11741609 (Pubitemid 34015963)
17. M Eberl M Hintz A Reichenberg AK Kollas J Wiesner H Jomaa 2003 Microbial isoprenoid biosynthesis and human γδ T cell activation FEBS Lett 544 4 10 10.1016/S0014-5793(03)00483-6 1:CAS:528:DC%2BD3sXktFWltLw%3D 12782281 (Pubitemid 36628027)
18. V Kunzmann E Bauer M Wilhelm 1999 γδ T-cell stimulation by pamidronate N Engl J Med 340 737 738 10.1056/NEJM199903043400914 1:STN:280:DyaK1M7ltVSrsQ%3D%3D 10068336 (Pubitemid 29110764)
19. HJ Gober M Kistowska L Angman P Jenö L Mori G De Libero 2003 Human T cell receptor γδ cells recognize endogenous mevalonate metabolites in tumor cells J Exp Med 197 163 168 10.1084/jem.20021500 1:CAS:528: DC%2BD3sXmt1Sjtg%3D%3D 12538656 (Pubitemid 36152311)
20. P Fisch M Malkovsky S Kovats E Sturm E Braakman BS Klein SD Voss LW Morrissey R DeMars WJ Welcj RLH Bolhuis PM Sondel 1990 Recognition by human Vγ9Vδ2 T cells of a GroEL homolog on Daudi Burkitt's lymphoma cells Science 250 1269 1273 10.1126/science.1978758 1:CAS:528:DyaK3MXktVKjtA%3D%3D 1978758
21. E Viey G Fromont B Escudier Y Morel S Da Rocha S Chouaib A Caignard 2005 Phosphostim-activated γδ T cells kill autologous metastatic renal cell carcinoma J Immunol 174 1338 1347 1:CAS:528:DC%2BD2MXlsFygsQ%3D%3D 15661891
22. SR Mattarollo T Kenna M Nieda AJ Nicol 2007 Chemotherapy and zoledronate sensitize solid tumour cells to Vγ9Vδ2 T cell cytotoxicity Cancer Immunol Immunother 56 1285 1297 10.1007/s00262-007-0279-2 1:CAS:528: DC%2BD2sXltlSks7k%3D 17265022 (Pubitemid 46763941)
23. P Vantourout J Mookerjee-Basu C Rolland F Pont H Martin C Davrinche LO Martinez B Perret X Collet C Périgaud S Peyrottes E Champagne 2009 Specific requirements for Vγ9Vδ2 T cell stimulation by a natural adenylated phosphoantigen J Immunol 183 3848 3857 10.4049/jimmunol.0901085 1:CAS:528:DC%2BD1MXhtVOmu77K 19710470
24. M Wilhelm V Kunzmann S Eckstein P Reimer F Weissinger T Ruediger HP Tony 2003 γδ T cells for immune therapy of patients with lymphoid malignancies Blood 102 200 206 10.1182/blood-2002-12-3665 1:CAS:528: DC%2BD3sXltFemurk%3D 12623838 (Pubitemid 36759655)
25. F Dieli D Vermijlen F Fulfaro N Caccamo S Meraviglia G Cicero A Roberts S Buccheri M D'Asaro N Gebbia A Salerno M Eberl AC Hayday 2007 Targeting human γδ T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer Cancer Res 67 7450 7457 10.1158/0008-5472. CAN-07-0199 1:CAS:528:DC%2BD2sXosVemtLY%3D 17671215 (Pubitemid 47206575)
26. J Bennouna E Bompas EM Neidhardt F Rolland I Philip C Galéa S Salot S Saiagh M Audrain M Rimbert S Lafaye-de Micheaux J Tiollier S Négrier 2008 Phase-I study of Innacell γδ, an autologous cell-therapy product highly enriched in γ9δ2 T lymphocytes, in combination with IL-2, in patients with metastatic renal cell carcinoma Cancer Immunol Immunother 57 1599 1609 10.1007/s00262-008-0491-8 1:CAS:528: DC%2BD1cXhtVejsbnK 18301889
27. H Kobayashi Y Tanaka J Yagi Y Osaka H Nakazawa T Uchiyama N Minato H Toma 2007 Safety profile and anti-tumor effects of adoptive immunotherapy using γδ T cells against advanced renal cell carcinoma: a pilot study Cancer Immunol Immunother 56 469 476 10.1007/s00262-006-0199-6 1:CAS:528:DC%2BD2sXht1yhsLg%3D 16850345 (Pubitemid 46204533)
28. CH June BR Blazar JL Riley 2009 Engineering lymphocyte subsets: tools, trials and tribulations Nat Rev Immunol 9 704 716 10.1038/nri2635 1:CAS:528:DC%2BD1MXhtFOhs77K 19859065
29. B Altincicek J Moll N Campos G Foerster E Beck JF Hoeffler C Grosdemange-Billiard M Rodríguez-Concepción M Rohmer A Boronat M Eberl H Jomaa 2001 Cutting edge: human γδ T cells are activated by intermediates of the 2-C-methyl-d-erythritol 4-phosphate pathway of isoprenoid biosynthesis J Immunol 166 3655 3658 1:CAS:528:DC%2BD3MXitVGntL0%3D 11238603
30. A Reichenberg M Hintz Y Kletschek T Kuhl C Haug R Engel J Moll DN Ostrovsky H Jomaa M Eberl 2003 Replacing the pyrophosphate group of HMB-PP by a diphosphonate function abrogates its potential to activate human γδ T cells but does not lead to competitive antagonism Bioorg Med Chem Lett 13 1257 1260 10.1016/S0960-894X(03)00138-0 1:CAS:528:DC%2BD3sXitlKjtL4%3D 12657258 (Pubitemid 36355933)
31. + natural T cells with distinct cytotoxic activities and Th1, Th2, and Th0 cytokine secretion patterns J Immunol 163 2314 2321 1:CAS:528:DyaK1MXltFagt74%3D 10438977
32. Dieli F, Poccia F, Lipp M, Sireci G, Caccamo N, Di Sano C, Salerno A (2003) Differentiation of effector/memory Vδ2 T cells and migratory routes in lymph nodes or inflammatory sites. J Exp Med 198:391-397
33. A Martino R Casetti A D'Alessandri A Sacchi F Poccia 2005 Complementary function of γδ T-lymphocytes and dendritic cells in the response to isopentenyl-pyrophosphate and lipopolysaccharide antigens J Clin Immunol 25 230 237 10.1007/s10875-005-4080-8 1:CAS:528:DC%2BD2MXnsVehtLc%3D 15981088 (Pubitemid 40884049)
34. MC Devilder S Allain C Dousset M Bonneville E Scotet 2009 Early triggering of exclusive IFN-γ responses of human Vγ9Vδ2 T cells by TLR-activated myeloid and plasmacytoid dendritic cells J Immunol 183 3625 3633 10.4049/jimmunol.0901571 1:CAS:528:DC%2BD1MXhtVOmurvN 19710464
35. A Bendelac PT Savage L Teyton 2007 The biology of NKT cells Annu Rev Immunol 25 297 336 10.1146/annurev.immunol.25.022106.141711 1:CAS:528: DC%2BD2sXltlansr4%3D 17150027 (Pubitemid 46697911)
36. R Nakagawa I Nagafune Y Tazunoki H Ehara H Tomura R Iijima K Motoki M Kamishohara S Seki 2001 Mechanisms of the antimetastatic effect in the liver and of the hepatocyte injury induced by α-galactosylceramide in mice J Immunol 166 6578 6584 1:CAS:528:DC%2BD3MXjvFartb4%3D 11359810
37. + T cells and natural killer cells is essential for the antimetastatic effect of α-galactosylceramide Blood 99 1259 1266 10.1182/blood.V99.4.1259 1:CAS:528:DC%2BD38XhtlWqsbo%3D 11830474 (Pubitemid 34547079)
38. J Kelly-Rogers L Madrigal-Estebas T O'Connor DG Doherty 2006 Activation-induced expression of CD56 by T cells is associated with a reprogramming of cytolytic activity and cytokine secretion profile in vitro Hum Immunol 67 863 873 10.1016/j.humimm.2006.08.292 1:CAS:528:DC%2BD28Xht1Kmt7jE 17145366 (Pubitemid 44828203)
39. F Gerosa B Baldani-Guerra C Nisii V Marchesini G Carra G Trinchieri 2002 Reciprocal activating interaction between natural killer cells and dendritic cells J Exp Med 195 327 333 10.1084/jem.20010938 1:CAS:528:DC%2BD38Xht1Wjt7o%3D 11828007 (Pubitemid 34461490)
40. H Kitamura K Iwakabe T Yahata S Nishimura A Ohta Y Ohmi M Sato K Takeda K Okumura L Van Kaer T Kawano M Taniguchi T Nishimura 1999 The natural killer T (NKT) cell ligand α-galactosylceramide demonstrates its immunopotentiating effect by inducing interleukin (IL)-12 production by dendritic cells and IL-12 receptor expression on NKT cells J Exp Med 189 1121 1128 10.1084/jem.189.7.1121 1:CAS:528:DyaK1MXitlemtrc%3D 10190903 (Pubitemid 29169829)
41. S Fujii K Shimizu C Smith L Bonifaz RM Steinman 2003 Activation of natural killer T cells by α-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a coadministered protein J Exp Med 198 267 279 10.1084/jem.20030324 1:CAS:528:DC%2BD3sXlvVyjtbo%3D 12874260 (Pubitemid 36987852)
42. MS Vincent DS Leslie JE Gumperz X Xiong EP Grant MB Brenner 2002 CD1-dependent dendritic cell instruction Nat Immunol 3 1163 1168 10.1038/ni851 1:CAS:528:DC%2BD38XovFChsbw%3D 12415264 (Pubitemid 35469701)
43. DS Leslie MS Vincent FM Spada H Das M Sugita CT Morita MB Brenner 2002 CD1-mediated γ/δ T cell maturation of dendritic cells J Exp Med 196 1575 1584 10.1084/jem.20021515 1:CAS:528:DC%2BD38XpslWlurc%3D 12486100 (Pubitemid 36026469)
44. M Terabe J Swann E Ambrosino P Sinha S Takaku Y Hayakawa DI Godfrey S Ostrand-Rosenberg MJ Smyth JA Berzofsky 2005 A nonclassical non- Vα14Jα18 CD1d-restricted (type II) NKT cell is sufficient for down-regulation of tumor immunosurveillance J Exp Med 202 1627 1633 10.1084/jem.20051381 1:CAS:528:DC%2BD2MXhtlCjsrvF 16365146 (Pubitemid 41815868)
45. MB Lutz G Schuler 2002 Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol 23 445 449 10.1016/S1471-4906(02)02281-0 1:CAS:528:DC%2BD38XmsVekuro%3D 12200066 (Pubitemid 35015188)
46. CT Morita EM Beckman JF Bukowski Y Tanaka H Band BR Bloom DE Golan MB Brenner 1995 Direct presentation of nonpeptide prenyl pyrophosphate antigens to human γδ T cells Immunity 3 495 507 10.1016/1074-7613(95)90178-7 1:CAS:528:DyaK2MXovFymsLk%3D 7584140
47. L Battistini N Caccamo G Borsellino S Meraviglia DF Angelini F Dieli MT Cencioni A Salerno 2005 Homing and memory patterns of human γδ T cells in physiopathological situations Microbes Infect 7 510 517 10.1016/j.micinf.2004.12.008 1:CAS:528:DC%2BD2MXjs1Oit7g%3D 15804491 (Pubitemid 40603451)
48. DV Correia F d'Orey BA Cardoso T Lança AR Grosso A deBarros LR Martins JT Barata B Silva-Santos 2009 Highly active microbial phosphoantigen induces rapid yet sustained MEK/Erk- and PI-3K/Akt-mediated signal transduction in anti-tumor human γδ T-cells PLoS One 4 e5657 10.1371/journal. pone.0005657 19479075