Phenotypic analysis of human peripheral blood regulatory T cells (CD4 +FOXP3+CD127lo/-) ex vivo and after in vitro restimulation with malaria antigens

European Journal of Immunology

Volumn 40, Issue 1, 2010, Pages 47-60

  Finney, Olivia C ^a,b,c   Riley, Eleanor M ^b   Walther, Michael ^a  

^a MEDICAL RESEARCH COUNCIL LABORATORIES   (Gambia)

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

^c SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

Human; Malaria; Regulation; Treg; Treg phenotype

Indexed keywords

CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR; CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR7; FAS ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 7 RECEPTOR; MALARIA ANTIGEN; PARASITE ANTIGEN; PROTEIN BCL 2; PROTEIN BNIP3; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; CHEMOKINE RECEPTOR; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; INTERLEUKIN 7 RECEPTOR ALPHA; PROTOZOAL PROTEIN;

ADULT; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CD4+ FOXP3+ T LYMPHOCYTE; CELL ACTIVATION; CELL MIGRATION; CELL POPULATION; EX VIVO STUDY; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IN VITRO STUDY; MEMORY CELL; NORMAL HUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; AGED; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MIDDLE AGED; PLASMODIUM FALCIPARUM;

ADULT; AGED; ANTIGENS, PROTOZOAN; APOPTOSIS; BIOLOGICAL MARKERS; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOLOGIC MEMORY; INTERLEUKIN-7 RECEPTOR ALPHA SUBUNIT; LYMPHOCYTE ACTIVATION; MIDDLE AGED; PHENOTYPE; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RECEPTORS, CHEMOKINE; T-LYMPHOCYTES, REGULATORY; YOUNG ADULT;

EID: 74249118677     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939708     Document Type: Article

References (81)

1. + Immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 Production. J. Exp. Med. 1998. 188: 287-296.
2. + immunoregulatory cells. J. Immunol. 2001. 167: 1137-1140.
3. + regulatory T cells suppress NKT cell functions. Cancer Res. 2003. 63: 4516-4520.
4. + regulatory T cells down-regulate co-stimulatory molecules on antigen-presenting cells. Eur. J. Immunol. 2000. 30: 1538-1543.
5. + regulatory T cells. Hum. Immunol. 2005. 66: 222-230.
6. + regulatory T cells. J. Immunol. 2005. 175: 4180-4183.
7. + regulatory T cells inhibit natural killer cell functions in a transforming growth factor-beta-dependent manner. J. Exp. Med. 2005. 202: 1075-1085.
8. Vignali, D., How many mechanisms do regulatory T cells need? Eur. J. Immunol. 2008. 38: 908-911.
9. Costantino, C. M., Baecher-Allan, C. M. and Hafler, D. A., Human regulatory T cells and autoimmunity. Eur. J. Immunol. 2008. 38: 921-924.
10. + T cells expressing the FoxP3 transcription factor. Immunity 2009. 30: 899-911.
11. Tadokoro, C. E., Shakhar, G., Shen, S., Ding, Y., Lino, A. C., Maraver, A., Lafaille, J. J. and Dustin, M. L., Regulatory T cells inhibit stable contacts between CD4+ T cells and dendritic cells in vivo. J. Exp. Med. 2006. 203: 505-511.
12. Tang, Q., Adams, J. Y., Tooley, A. J., Bi, M., Fife, B. T., Serra, P., Santamaria, P. et al., Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat. Immunol. 2006. 7: 83-92.
13. Lim, H.W., Hillsamer, P. and Kim, C. H., Regulatory T cells can migrate to follicles upon T cell activation and suppress GC-Th cells and GC-Th cell-driven B cell responses. J. Clin. Invest. 2004. 114: 1640-1649.
14. Bai, Y., Liu, J., Wang, Y., Honig, S., Qin, L., Boros, P. and Bromberg, J. S., L-selectin-dependent lymphoid occupancy is required to induce alloantigen-specific tolerance. J. Immunol. 2002. 168: 1579-1589.
15. + T cells. Int. Immunol. 2003. 15: 731-739.
16. + regulatory T cells in the regional lymph node. J. Exp. Med. 2005. 202: 771-781.
17. + T cells in skin lesions of patients with cutaneous leishmaniasis exhibit phenotypic and functional characteristics of natural regulatory T cells. J. Infect. Dis. 2006. 193: 1313-1322.
18. Salhi, A., Rodrigues, V., Jr., Santoro, F., Dessein, H., Romano, A., Castellano, L. R., Sertorio, M. et al., Immunological and genetic evidence for a crucial role of IL-10 in cutaneous lesions in humans infected with Leishmania braziliensis. J. Immunol. 2008. 180: 6139-6148.
19. + natural regulatory T cells are specific for microbial antigens. J. Exp. Med. 2006. 203: 777-788.
20. Epple, H. J., Loddenkemper, C., Kunkel, D., Troeger, H., Maul, J., Moos, V., Berg, E. et al., Mucosal but not peripheral FOXP3+ regulatory T cells are highly increased in untreated HIV infection and normalize after suppressive HAART. Blood 2006. 108: 3072-3078.
21. Guyot-Revol, V., Innes, J. A., Hackforth, S., Hinks, T. and Lalvani, A., Regulatory T cells are expanded in blood and disease sites in patients with tuberculosis. Am. J. Respir. Crit. Care Med. 2006. 173: 803-810.
22. Hougardy, J. M., Place, S., Hildebrand, M., Drowart, A., Debrie, A. S., Locht, C. and Mascart, F., Regulatory T cells depress immune responses to protective antigens in active tuberculosis. Am. J. Respir. Crit. Care Med. 2007. 176: 409-416.
23. + T cells in regulation of the immune response during human tuberculosis. Clin. Exp. Immunol. 2006. 144: 25-34.
24. Cavassani, K. A., Campanelli, A. P.,Moreira, A. P., Vancim, J. O., Vitali, L. H., Mamede, R. C., Martinez, R. and Silva, J. S., Systemic and local characterization of regulatory T cells in a chronic fungal infection in humans. J. Immunol. 2006. 177: 5811-5818.
25. + regulatory T cells specific for human papillomavirus antigens. Proc. Natl. Acad. Sci. 2007. 104: 12087-12092.
26. + splenocytes that delays adoptive transfer of diabetes expresses L-selectin and high levels of CCR7. J. Immunol. 2002. 169: 2461-2465.
27. + T regulatory cells mediating allograft tolerance depends on the CCR4 chemokine receptor. J. Exp. Med. 2005. 201: 1037-1044.
28. Ishida, T., Ishii, T., Inagaki, A., Yano, H., Komatsu, H., Iida, S., Inagaki, H. and Ueda, R., Specific recruitment of CC chemokine receptor 4-positive regulatory T cells in Hodgkin lymphoma fosters immune privilege. Cancer Res. 2006. 66: 5716-5722.
29. + T cells in B-cell non-Hodgkin lymphoma. Blood 2006. 107: 3639-3646.
30. + regulatory T cells during acute graft-versus-host disease. Blood 2005. 106: 3300-3307.
31. + T-cell subset. Blood 2005. 105: 2877-2886.
32. + regulatory T cells. J. Immunol. 2006. 177: 840-851.
33. + T cells represent major subsets of human peripheral blood memory T cells migrating in response to CCL1/I-309. Eur. J. Immunol. 2002. 32: 3506-3514.
34. + regulatory T cells bear functional skin-homing receptors. J. Immunol. 2006. 177: 4488-4494.
35. Iellem, A., Mariani, M., Lang, R., Recalde, H., Panina-Bordignon, P., Sinigaglia, F. and D'Ambrosio,D., Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4 (+)CD25(+) regulatory T cells. J. Exp. Med. 2001. 194: 847-853.
36. Eksteen, B., Miles, A., Curbishley, S. M., Tselepis, C., Grant, A. J., Walker, L. S. K. and Adams, D. H., Epithelial inflammation is associated with CCL28 production and the recruitment of regulatory T cells expressing CCR10. J. Immunol. 2006. 177: 593-603.
37. + Tregs. Clin. Immunol. 2008. 126: 291-302.
38. Finney, O. C., Nwakanma, D., Conway, D. J., Walther, M. and Riley, E. M., Homeostatic regulation of T effector to Treg ratios in an area of seasonal malaria transmission. Eur. J. Immunol. 2009. 39: 1288-1300.
39. Taams, L. S., Smith, J., Rustin, M. H., Salmon, M., Poulter, L. W. and Akbar, A. N., Human anergic/suppressive CD4(+)CD25(+) T cells: a highly differentiated and apoptosis-prone population. Eur. J. Immunol. 2001. 31: 1122-1131.
40. + regulatory T cells are highly susceptible to CD95 ligand- but not to TCR-mediated cell death. J. Immunol. 2005. 175: 32-36.
41. Fritzsching, B., Oberle, N., Pauly, E., Geffers, R., Buer, J., Poschl, J., Krammer, P. et al., Naive regulatory T cells: a novel subpopulation defined by resistance toward CD95L-mediated cell death. Blood 2006. 108: 3371-3378.
42. + regulatory T cells are derived by rapid turnover of memory populations in vivo. J. Clin. Invest. 2006. 116: 2423-2433.
43. Seddiki, N., Santner-Nanan, B., Martinson, J., Zaunders, J., Sasson, S., Landay, A., Solomon, M. et al., Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. J. Exp. Med. 2006. 203: 1693-1700.
44. Walther, M., Tongren, J. E., Andrews, L., Korbel, D., King, E., Fletcher, H., Andersen, R. F. et al., Upregulation of TGF-beta, FOXP3, and CD4(+) CD25(+) regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 2005. 23: 287-296.
45. + regulatory T cells following anti-CD25 treatment in malaria-infected mice. J. Immunol. 2007. 178: 4136-4146.
46. Couper, K. N., Blount, D. G., Wilson, M. S., Hafalla, J. C., Belkaid, Y., Kamanaka, M., Flavell, R. A. et al., IL-10 from CD4CD25Foxp3CD127 adaptive regulatory T cells modulates parasite clearance and pathology during malaria infection. PLoS Pathog. 2008. 4: e1000004.
47. Walther, M., Jeffries, D., Finney, O. C., Njie, M., Ebonyi, A., Deininger, S., Lawrence, E. et al., Distinct roles for FOXP3 and FOXP3 CD4 T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. PLoS Pathog. 2009. 5: e1000364.
48. high regulatory cells in human peripheral blood. J. Immunol. 2001. 167: 1245-1253.
49. + T cells with regulatory properties isolated from peripheral blood. J. Exp. Med. 2001. 193: 1285-1294.
50. Valmori, D., Merlo, A., Souleimanian, N. E., Hesdorffer, C. S. and Ayyoub, M., A peripheral circulating compartment of natural naive CD4 Tregs. J. Clin. Invest. 2005. 115: 1953-1962.
51. Campbell, J. J., Murphy, K. E., Kunkel, E. J., Brightling, C. E., Soler, D., Shen, Z., Boisvert, J. et al., CCR7 expression and memory T cell diversity in humans. J. Immunol. 2001. 166: 877-884.
52. Sallusto, F., Lenig, D., Forster, R., Lipp, M. and Lanzavecchia, A., Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999. 401: 708-712.
53. Andrew, D. P., Ruffing, N., Kim, C. H., Miao, W., Heath, H., Li, Y., Murphy, K. et al., C-C chemokine receptor 4 expression defines a major subset of circulating nonintestinal memory T cells of both Th1 and Th2 potential. J. Immunol. 2001. 166: 103-111.
54. Campbell, J. J., Haraldsen, G., Pan, J., Rottman, J., Qin, S., Ponath, P., Andrew, D. P. et al., The chemokine receptor CCR4 in vascular recognition by cutaneous but not intestinal memory T cells. Nature 1999. 400: 776-780.
55. Sprent, J. and Tough, D. F., Lymphocyte life-span and memory. Science 1994. 265: 1395-1400.
56. Jameson, S. C., T cell homeostasis: keeping useful T cells alive and live T cells useful. Semin. Immunol. 2005. 17: 231-237.
57. + T reg cells. J. Exp. Med. 2006. 203: 1701-1711.
58. Fontenot, J. D., Rasmussen, J. P., Gavin, M. A. and Rudensky, A. Y., A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 2005. 6: 1142-1151.
59. high T Cells in Type 1 diabetes may be partially mediated by IL-2 deprivation. PLoS ONE 2009. 4: e6527.
60. + regulatory T cells upon repetitive in vitro stimulation. Eur. J. Immunol. 2009. 39: 1088-1097.
61. Scholzen, A., Mittag, D., Rogerson, S. J., Cooke, B. M. and Plebanski, M., Plasmodium falciparum-mediated induction of human CD25Foxp3 CD4 T cells is independent of direct TCR stimulation and requires IL-2, IL-10 and TGFbeta. PLoS Pathog. 2009. 5: e1000543.
62. Shimizu, J., Yamazaki, S., Takahashi, T., Ishida, Y. and Sakaguchi, S., Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat. Immunol. 2002. 3: 135-142.
63. McHugh, R. S., Whitters, M. J., Piccirillo, C. A., Young, D. A., Shevach, E. M., Collins, M. and Byrne, M. C., CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 2002. 16: 311-323.
64. Read, S., Malmstrom, V. and Powrie, F., Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25 (+)CD4(+) regulatory cells that control intestinal inflammation. J. Exp. Med. 2000. 192: 295-302.
65. + human thymocytes. J. Exp. Med. 2002. 196: 379-387.
66. + regulatory T cells in adult life. Blood 2006. 107: 2830-2838.
67. + regulatory T cells. Immunology 2003. 109: 319-325.
68. + T cells from HIV-infected patients responding to antiretroviral therapy. Immunol. Cell Biol. 2006. 84: 530-536.
69. Katou, F., Ohtani, H., Nakayama, T., Ono, K.,Matsushima, K., Saaristo, A., Nagura, H. et al., Macrophage-derived chemokine (MDC/CCL22) and CCR4 are involved in the formation of T lymphocyte-dendritic cell clusters in human inflamed skin and secondary lymphoid tissue. Am. J. Pathol. 2001. 158: 1263-1270.
70. Tarbell, K. V., Yamazaki, S. and Steinman, R. M., The interactions of dendritic cells with antigen-specific, regulatory T cells that suppress autoimmunity. Semin. Immunol. 2006. 18: 93-102.
71. Onishi, Y., Fehervari, Z., Yamaguchi, T. and Sakaguchi, S., Foxp3+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc. Natl. Acad. Sci. USA 2008. 105: 10113-10118.
72. Urban, B. C., Ferguson, D. J. P., Pain, A., Willcox, N., Plebanski, M., Austyn, J. M. and Roberts, D. J., Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 1999. 400: 73-77.
73. Urban, B. C. and Roberts, D. J., Malaria, monocytes, macrophages and myeloid dendritic cells: sticking of infected erythrocytes switches off host cells. Curr. Opin. Immunol. 2002. 14: 458-465.
74. + T cells undergo conventional first switch to lymphoid tissue homing receptors in thymus but accelerated second switch to nonlymphoid tissue homing receptors in secondary lymphoid tissues. J. Immunol. 2007. 178: 301-311.
75. Akbar, A. N., Salmon, M., Savill, J. and Janossy, G., A possible role for bcl-2 in regulating T-cell memory - a 'balancing act' between cell death and survival. Immunol. Today 1993. 14: 526-532.
76. + T cells in the periphery. Nat. Rev. Immunol. 2007. 7: 231-237.
77. Krammer, P. H., CD95's deadly mission in the immune system. Nature 2000. 407: 789-795.
78. Rathmell, J. C. and Thompson, C. B., Pathways of apoptosis in lymphocyte development, homeostasis, and disease. Cell 2002. 109 S97-S107.
79. Brandenburg, S., Takahashi, T., de la Rosa, M., Janke, M., Karsten, G., Muzzulini, T., Orinska, Z. et al., IL-2 induces in vivo suppression by CD4(+)CD25(+)Foxp3(+) regulatory T cells. Eur. J. Immunol. 2008. 38: 1643-1653.
80. Akbar, A. N., Borthwick, N., Salmon, M., Gombert, W., Bofill, M., Shamsadeen, N., Pilling, D. et al., The significance of low bcl-2 expression by CD45RO T cells in normal individuals and patients with acute viral infections. The role of apoptosis in T cell memory. J. Exp. Med. 1993. 178: 427-438.
81. Trager, W. and Jensen, J. B., Human malaria parasites in continuous culture. Science 1976. 193: 673-675.