Upregulation of TGF-β, FOXP3, and CD4+CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection

Immunity

Volumn 23, Issue 3, 2005, Pages 287-296

  Walther, Michael ^a,e   Tongren, Jon Eric ^b,f   Andrews, Laura ^a   Korbel, Daniel ^b   King, Elizabeth ^b   Fletcher, Helen ^a   Andersen, Rikke F ^a   Bejon, Philip ^a   Thompson, Fiona ^a   Dunachie, Susanna J ^a   Edele, Fanny ^b,g   De Souza, J Brian ^b,c   Sinden, Robert E ^d   Gilbert, Sarah C ^a   Riley, Eleanor M ^b   Hill, Adrian V S ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^c ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e MEDICAL RESEARCH COUNCIL LABORATORIES   (Gambia)

^f CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^g UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CYTOKINE; INTERLEUKIN 2 RECEPTOR ALPHA; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; VIRULENCE FACTOR;

ADULT; ANTIGEN SPECIFICITY; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LONGITUDINAL STUDY; MALARIA; PARASITE DEVELOPMENT; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTOZOAL INFECTION; SPOROZOITE; T LYMPHOCYTE; UPREGULATION;

ANIMALS; ANTIGENS, CD4; CLINICAL TRIALS; DNA-BINDING PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; RECEPTORS, INTERLEUKIN-2; T-LYMPHOCYTES; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

EID: 24944466472     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2005.08.006     Document Type: Article

References (58)

1. + regulatory T cells control T-cell responses to human immunodeficiency virus and cytomegalovirus antigens J. Virol. 78 2004 2454 2459
2. L. Andrews, R.F. Andersen, D. Webster, S. Dunachie, R.M. Walther, P. Bejon, A. Hunt-Cooke, G. Bergson, F. Sanderson, A.B. Hill, and S.C. Gilbert Quantitative real-time polymerase chain reaction for malaria diagnosis and its use in malaria vaccine clinical trials Am. J. Trop. Med. Hyg. 73 2005 191 198
3. K. Artavanis-Tsakonas, and E.M. Riley Innate immune response to malaria: rapid induction of IFN-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes J. Immunol. 169 2002 2956 2963
4. high regulatory cells in human peripheral blood J. Immunol. 167 2001 1245 1253
5. + T cells Clin. Immunol. 115 2005 10 18
6. F.J. Barrat, D.J. Cua, A. Boonstra, D.F. Richards, C. Crain, H.F. Savelkoul, R. de Waal-Malefyt, R.L. Coffman, C.M. Hawrylowicz, and A. O'Garra In vitro generation of interleukin 10-producing regulatory CD4(+) T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)- and Th2-inducing cytokines J. Exp. Med. 195 2002 603 616
7. P. Bejon, L. Andrews, R.F. Andersen, S. Dunachie, D. Webster, M. Walther, S.C. Gilbert, T. Peto, and A.V.S. Hill Calculation of liver-to-blood inocula, parasite growth rates and pre-erythrocytic vaccine efficacy, from serial quantitative PCR studies of volunteers challenged with malaria sporozoite J. Infect. Dis. 191 2005 619 626
8. + regulatory T cells control Leishmania major persistence and immunity Nature 420 2002 502 507
9. M.E. Brunkow, E.W. Jeffery, K.A. Hjerrild, B. Paeper, L.B. Clark, S.A. Yasayko, J.E. Wilkinson, D. Galas, S.F. Ziegler, and F. Ramsdell Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse Nat. Genet. 27 2001 68 73
10. R. Cabrera, Z. Tu, Y. Xu, R.J. Firpi, H.R. Rosen, C. Liu, and D.R. Nelson An immunomodulatory role for CD4(+)CD25(+) regulatory T lymphocytes in hepatitis C virus infection Hepatology 40 2004 1062 1071
11. S.C. Chaiyaroj, A.S. Rutta, K. Muenthaisong, P. Watkins, M. Na Ubol, and S. Looareesuwan Reduced levels of transforming growth factor-beta1, interleukin-12 and increased migration inhibitory factor are associated with severe malaria Acta Trop. 89 2004 319 327
12. Y. Chen, V.K. Kuchroo, J. Inobe, D.A. Hafler, and H.L. Weiner Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis Science 265 1994 1237 1240
13. + regulatory T cells by TGF-beta induction of transcription factor Foxp3 J. Exp. Med. 198 2003 1875 1886
14. J.B. de Souza, and E.M. Riley Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis Microbes Infect. 4 2002 291 300
15. D. Dieckmann, H. Plottner, S. Berchtold, T. Berger, and G. Schuler Ex vivo isolation and characterization of CD4(+)CD25(+) T cells with regulatory properties from human blood J. Exp. Med. 193 2001 1303 1310
16. D. Dieckmann, C.H. Bruett, H. Ploettner, M.B. Lutz, and G. Schuler Human CD4(+)CD25(+) regulatory, contact-dependent T cells induce interleukin 10-producing, contact-independent type 1-like regulatory T cells J. Exp. Med. 196 2002 247 253
17. D. Dodoo, F.M. Omer, J. Todd, B.D. Akanmori, K.A. Koram, and E.M. Riley Absolute levels and ratios of proinflammatory and anti-inflammatory cytokine production in vitro predict clinical immunity to Plasmodium falciparum malaria J. Infect. Dis. 185 2002 971 979
18. L. Fahlen, S. Read, L. Gorelik, S.D. Hurst, R.L. Coffman, R.A. Flavell, and F. Powrie T cells that cannot respond to TGF-beta escape control by CD4(+)CD25(+) regulatory T cells J. Exp. Med. 201 2005 737 746
19. - T cells through Foxp3 induction and down-regulation of Smad7 J. Immunol. 172 2004 5149 5153
20. + regulatory T cells Nat. Immunol. 4 2003 330 336
21. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis Nature 389 1997 737 742
22. + regulatory T cells Nat. Med. 10 2004 29 30
23. S. Hori, T. Nomura, and S. Sakaguchi Control of regulatory T cell development by the transcription factor Foxp3 Science 299 2003 1057 1061
24. H. Jonuleit, E. Schmitt, M. Stassen, A. Tuettenberg, J. Knop, and A.H. Enk Identification and functional characterization of human CD4(+)CD25(+) T cells with regulatory properties isolated from peripheral blood J. Exp. Med. 193 2001 1285 1294
25. H. Jonuleit, E. Schmitt, H. Kakirman, M. Stassen, J. Knop, and A.H. Enk Infectious tolerance: human CD25(+) regulatory T cells convey suppressor activity to conventional CD4(+) T helper cells J. Exp. Med. 196 2002 255 260
26. + T regulatory cells Nat. Immunol. 4 2003 337 342
27. A.L. Kinter, M. Hennessey, A. Bell, S. Kern, Y. Lin, M. Daucher, M. Planta, M. McGlaughlin, R. Jackson, S.F. Ziegler, and A.S. Fauci CD25(+)CD4(+) regulatory T cells from the peripheral blood of asymptomatic HIV-infected individuals regulate CD4(+) and CD8(+) HIV-specific T cell immune responses in vitro and are associated with favorable clinical markers of disease status J. Exp. Med. 200 2004 331 343
28. Y. Laouar, F.S. Sutterwala, L. Gorelik, and R.A. Flavell Transforming growth factor-beta controls T helper type 1 cell development through regulation of natural killer cell interferon-gamma Nat. Immunol. 6 2005 600 607
29. M.K. Levings, R. Sangregorio, and M.G. Roncarolo Human cd25(+)cd4(+) t regulatory cells suppress naive and memory T cell proliferation and can be expanded in vitro without loss of function J. Exp. Med. 193 2001 1295 1302
30. C. Li, L.A. Sanni, F. Omer, E. Riley, and J. Langhorne Pathology of Plasmodium chabaudi chabaudi infection and mortality in interleukin-10-deficient mice are ameliorated by anti-tumor necrosis factor alpha and exacerbated by anti-transforming growth factor beta antibodies Infect. Immun. 71 2003 4850 4856
31. high regulatory T cells suppress memory T-cell responses to H. pylori in infected individuals Infect. Immun. 71 2003 1755 1762
32. + regulatory T cells J. Exp. Med. 201 2005 1061 1067
33. S.J. McConkey, W.H. Reece, V.S. Moorthy, D. Webster, S. Dunachie, G. Butcher, J.M. Vuola, T.J. Blanchard, P. Gothard, and K. Watkins Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans Nat. Med. 9 2003 729 735
34. S. Mendez, S.K. Reckling, C.A. Piccirillo, D. Sacks, and Y. Belkaid Role for CD4(+) CD25(+) regulatory T cells in reactivation of persistent leishmaniasis and control of concomitant immunity J. Exp. Med. 200 2004 201 210
35. F.M. Omer, and E.M. Riley Transforming growth factor beta production is inversely correlated with severity of murine malaria infection J. Exp. Med. 188 1998 39 48
36. F.M. Omer, J.B. de Souza, P.H. Corran, A.A. Sultan, and E.M. Riley Activation of transforming growth factor beta by malaria parasite-derived metalloproteinases and a thrombospondin-like molecule J. Exp. Med. 198 2003 1817 1827
37. F.M. Omer, J.B. de Souza, and E.M. Riley Differential induction of TGF-beta regulates proinflammatory cytokine production and determines the outcome of lethal and nonlethal Plasmodium yoelii infections J. Immunol. 171 2003 5430 5436
38. - T cells Int. Immunol. 16 2004 1203 1213
39. D.J. Perkins, J.B. Weinberg, and P.G. Kremsner Reduced interleukin-12 and transforming growth factor-beta1 in severe childhood malaria: relationship of cytokine balance with disease severity J. Infect. Dis. 182 2000 988 992
40. J.A. Perry, C.S. Olver, R.C. Burnett, and A.C. Avery Cutting edge: the acquisition of TLR tolerance during malaria infection impacts T cell activation J. Immunol. 174 2005 5921 5925
41. F. Powrie, S. Read, C. Mottet, H. Uhlig, and K. Maloy Control of immune pathology by regulatory T cells Novartis Found. Symp. 252 2003 92 98
42. M.S. Rhee, B.D. Akanmori, M. Waterfall, and E.M. Riley Changes in cytokine production associated with acquired immunity to Plasmodium falciparum malaria Clin. Exp. Immunol. 126 2001 503 510
43. B.T. Rouse, and S. Suvas Regulatory cells and infectious agents: detentes cordiale and contraire J. Immunol. 173 2004 2211 2215
44. S. Sakaguchi, N. Sakaguchi, M. Asano, M. Itoh, and M. Toda Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases J. Immunol. 155 1995 1151 1164
45. J. Satoguina, M. Mempel, J. Larbi, M. Badusche, C. Loliger, O. Adjei, G. Gachelin, B. Fleischer, and A. Hoerauf Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis) Microbes Infect. 4 2002 1291 1300
46. + T-cell pool and the expression of Foxp3 in vivo Int. Immunol. 16 2004 1241 1249
47. L.A. Schubert, E. Jeffery, Y. Zhang, F. Ramsdell, and S.F. Ziegler Scurfin (FOXP3) acts as a repressor of transcription and regulates T cell activation J. Biol. Chem. 276 2001 37672 37679
48. L.A. Stephens, C. Mottet, D. Mason, and F. Powrie Human CD4(+)CD25(+) thymocytes and peripheral T cells have immune suppressive activity in vitro Eur. J. Immunol. 31 2001 1247 1254
49. K. Sugimoto, F. Ikeda, J. Stadanlick, F.A. Nunes, H.J. Alter, and K.M. Chang Suppression of HCV-specific T cells without differential hierarchy demonstrated ex vivo in persistent HCV infection Hepatology 38 2003 1437 1448
50. + regulatory T cells control the severity of viral immunoinflammatory lesions J. Immunol. 172 2004 4123 4132
51. L.S. Taams, J. Smith, M.H. Rustin, M. Salmon, L.W. Poulter, and A.N. Akbar Human anergic/suppressive CD4(+)CD25(+) T cells: a highly differentiated and apoptosis-prone population Eur. J. Immunol. 31 2001 1122 1131
52. + immunoregulatory T cells is antigen nonspecific J. Immunol. 164 2000 183 190
53. N. Tsutsui, and T. Kamiyama Transforming growth factor beta-induced failure of resistance to infection with blood-stage Plasmodium chabaudi in mice Infect. Immun. 67 1999 2306 2311
54. B.C. Urban, D.J. Ferguson, A. Pain, N. Willcox, M. Plebanski, J.M. Austyn, and D.J. Roberts Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells Nature 400 1999 73 77
55. M.A. van Waarde, A.J. van Assen, H.H. Kampinga, A.W. Konings, and Z. Vujaskovic Quantification of transforming growth factor-beta in biological material using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct Anal. Biochem. 247 1997 45 51
56. C. Wenisch, B. Parschalk, H. Burgmann, S. Looareesuwan, and W. Graninger Decreased serum levels of TGF-beta in patients with acute Plasmodium falciparum malaria J. Clin. Immunol. 15 1995 69 73
57. + regulatory T cells Int. Immunol. 16 2004 1643 1656
58. - cells to develop suppressive activity: the role of IL-2, TGF-beta, and IL-10 J. Immunol. 172 2004 5213 5221