Inhibition of activation induced CD154 on CD4 CD25 cells: A valid surrogate for human Treg suppressor function

Immunology and Cell Biology

Volumn 90, Issue 8, 2012, Pages 812-821

  Hill, Danika ^a,b   Eastaff Leung, Nicola ^a,b   Bresatz Atkins, Suzanne ^a,b   Warner, Noel ^c   Ruitenberg, Joyce ^c   Krumbiegel, Doreen ^b   Pederson, Steve ^a,b   Mcinnes, Natasha ^a   Brown, Cheryl Y ^a   Sadlon, Timothy ^a   Barry, Simon C ^a,b,d  

^a WOMEN S AND CHILDREN S HOSPITAL   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

^c 3BD Biosciences ^*  (United States)

^d UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

functional assays; iTreg; nTreg; regulatory T cells

Indexed keywords

CD40 LIGAND; TRANSCRIPTION FACTOR FOXP3;

ARTICLE; AUTOIMMUNITY; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CELL FUNCTION; CELL POPULATION; CELL PROLIFERATION; HIGH THROUGHPUT SCREENING; HOMEOSTASIS; HUMAN; HUMAN CELL; MALE; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE;

ADULT; CD40 LIGAND; CELL LINE; CELL MEMBRANE; CELL PROLIFERATION; FETAL BLOOD; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOASSAY; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE TEST, MIXED; MALE; PHENOTYPE; STAINING AND LABELING; T-LYMPHOCYTES, REGULATORY;

EID: 84866364885     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2012.18     Document Type: Article

References (45)

1. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. 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 1995; 155: 1151-1164.
2. Sakaguchi S. Naturally arising Foxp3-expressing CD25CD4 regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 2005; 6: 345-352.
3. Kim JM, Rasmussen JP, Rudensky AY. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol 2007; 8: 191-197.
4. Van Parijs L, Abbas AK. Homeostasis and self-tolerance in the immune system: Turning lymphocytes off. Science 1998; 280: 243-248.
5. Powrie F, Read S, Mottet C, Uhlig H, Maloy K. Control of immune pathology by regulatory T cells. Novartis Found Symp 2003; 252: 92-8; discussion 98-105, 106-114.
6. Bluestone JA, Tang Q, Sedwick CE. T regulatory cells in autoimmune diabetes: Past challenges, future prospects. J Clin Immunol 2008; 28: 677-684.
7. Eastaff-Leung N, Mabarrack N, Barbour A, Cummins A, Barry S. Foxp3 regulatory T cells, Th17 effector cells, and cytokine environment in inflammatory bowel disease. J Clin Immunol 2010; 30: 80-89.
8. Sarkar S, Fox DA. Regulatory T cells in rheumatoid arthritis. Curr Rheumatol Rep 2008; 10: 405-412.
9. Viglietta V, Baecher-Allan C, Weiner HL, Hafler DA. Loss of functional suppression by CD4CD25 regulatory T cells in patients with multiple sclerosis. J Exp Med 2004; 199: 971-979.
10. Liu W, Putnam AL, Xu-Yu Z, Szot GL, Lee MR, Zhu S et al. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4 T reg cells. J ExpMed 2006; 203: 1701-1711.
11. Feuerer M, Hill JA, Mathis D, Benoist C. Foxp3 regulatory T cells: Differentiation, specification, subphenotypes. Nat Immunol 2009; 10: 689-695.
12. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N et al. Conversion of peripheral CD4CD25- naive T cells to CD4CD25 regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 2003; 198: 1875-1886.
13. Chen Q, Kim YC, Laurence A, Punkosdy GA, Shevach EM. IL-2 controls the stability of Foxp3 expression in TGF-beta-induced Foxp3 T cells in vivo. J Immunol 2011; 186: 6329-6337.
14. Hill JA, Hall JA, Sun CM, Cai Q, Ghyselinck N, Chambon P et al. Retinoic acid enhances Foxp3 induction indirectly by relieving inhibition from CD4CD44hi Cells. Immunity 2008; 29: 758-770.
15. Marson A, Kretschmer K, Frampton GM, Jacobsen ES, Polansky JK, MacIsaac KD et al. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 2007; 445: 931-935.
16. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299: 1057-1061.
17. Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko SA et al. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 2001; 27: 68-73.
18. Bennett CL, Christie J, Ramsdell F, Brunkow ME, Ferguson PJ, Whitesell L et al. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 2001; 27: 20-21.
19. Wildin RS, Ramsdell F, Peake J, Faravelli F, Casanova JL, Buist N et al. X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy. Nat Genet 2001; 27: 18-20.
20. Williams LM, Rudensky AY. Maintenance of the Foxp3-dependent developmental program in mature regulatory T cells requires continued expression of Foxp3. Nat Immunol 2007; 8: 277-284.
21. Miyara M, Yoshioka Y, Kitoh A, Shima T, Wing K, Niwa A et al. Functional delineation and differentiation dynamics of human CD4 T cells expressing the FoxP3 transcription factor. Immunity 2009; 30: 899-911.
22. Sadlon TJ, Wilkinson BG, Pederson S, Brown CY, Bresatz S, Gargett T et al. Genomewide identification of human FOXP3 target genes in natural regulatory T cells. J Immunol 2010; 185: 1071-1081.
23. Zheng Y, Josefowicz SZ, Kas A, Chu TT, Gavin MA, Rudensky AY. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory Tcells. Nature 2007; 445: 936-940.
24. Pillai V, Ortega SB, Wang CK, Karandikar NJ. Transient regulatory T-cells: A state attained by all activated human T-cells. Clin Immunol 2007; 123: 18-29.
25. Wang J, Ioan-Facsinay A, van der Voort EI, Huizinga TW, Toes RE. Transient expression of FOXP3 in human activated nonregulatory CD4 T cells. Eur J Immunol 2007; 37: 129-138.
26. Bresatz S, Sadlon T, Millard D, Zola H, Barry SC. Isolation, propagation and characterization of cord blood derived CD4 CD25 regulatory T cells. J Immunol Methods 2007; 327: 53-62.
27. Banchereau J, Bazan F, Blanchard D, Briere F, Galizzi JP, van Kooten C et al. The CD40 antigen and its ligand. Annu Rev Immunol 1994; 12: 881-922.
28. Chattopadhyay PK, Yu J, Roederer M. A live-cell assay to detect antigen-specific CD4 T cells with diverse cytokine profiles. Nat Med 2005; 11: 1113-1117.
29. Chattopadhyay PK, Yu J, Roederer M. Live-cell assay to detect antigen-specific CD4 T-cell responses by CD154 expression. Nat Protoc 2006; 1: 1-6.
30. Lee SP, Ataga KI, Orringer EP, Phillips DR, Parise LV. Biologically active CD40 ligand is elevated in sickle cell anemia: Potential role for platelet-mediated inflammation. Arterioscler Thromb Vasc Biol 2006; 26: 1626-1631.
31. Foy TM, Page DM, Waldschmidt TJ, Schoneveld A, Laman JD, Masters SR et al. An essential role for gp39, the ligand for CD40, in thymic selection. J Exp Med 1995; 182: 1377-1388.
32. Ruitenberg JJ, Boyce C, Hingorani R, Putnam A, Ghanekar SA. Rapid assessment of in vitro expanded human regulatory T cell function. J Immunol Methods 2011: 1-12.
33. Hoffmann P, Eder R, Boeld TJ, Doser K, Piseshka B, Andreesen R et al. Only the CD45RA subpopulation of CD4CD25high T cells gives rise to homogeneous regulatory T-cell lines upon in vitro expansion. Blood 2006; 108: 4260-4267.
34. Wolke C, Tadje J, Bukowska A, Tager M, Bank U, Ittenson A et al. Assigning the phenotype of a natural regulatory T-cell to the human T-cell line, KARPAS-299. Int J Mol Med 2006; 17: 275-278.
35. Last'ovicka J, Budinsky V, Spisek R, Bartunkova J. Assessment of lymphocyte proliferation: CFSE kills dividing cells and modulates expression of activation markers. Cell Immunol 2009; 256: 79-85.
36. Ozdemir O. Evaluation of human mast cell-mediated cytotoxicity by DIOC18 target cell labeling in flow cytometry. J Immunol Methods 2007; 319: 98-103.
37. Itoh M, Takahashi T, Sakaguchi N, Kuniyasu Y, Shimizu J, Otsuka F et al. Thymus and autoimmunity: Production of CD25CD4 naturally anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J Immunol 1999; 162: 5317-5326.
38. Hoffmann P, Eder R, Kunz-Schughart LA, Andreesen R, Edinger M. Large-scale in vitro expansion of polyclonal human CD4()CD25high regulatory T cells. Blood 2004; 104: 895-903.
39. Ukena SN, Hopting M, Velaga S, Ivanyi P, Grosse J, Baron U et al. Isolation strategies of regulatory T cells for clinical trials: Phenotype, function, stability, and expansion capacity. Exp Hematol 2011; 39: 1152-1160.
40. d'Hennezel E, Yurchenko E, Sgouroudis E, Hay V, Piccirillo CA. Single-cell analysis of the human T regulatory population uncovers functional heterogeneity and instability within FOXP3 cells. J Immunol 2011; 186: 6788-6797.
41. Jana S, Campbell H, Woodliff J, Waukau J, Jailwala P, Ghorai J et al. The type of responder T-cell has a significant impact in a human in vitro suppression assay. PLoS One 2010; 5: E15154.
42. Baecher-Allan CM, Hafler DA. Functional analysis of highly defined, FACS-isolated populations of human regulatory CD4CD25 T cells. Clin Immunol 2005; 117: 192. discussion 193.
43. Hoffmann HJ, Malling TM, Topcu A, Ryder LP, Nielsen KR, Varming K et al. CD4dimCD25bright Treg cell frequencies above a standardized gating threshold are similar in asthmatics and controls. Cytometry A 2007; 71: 371-378.
44. Ukena SN, Velaga S, Geffers R, Grosse J, Baron U, Buchholz S et al. Human regulatory T cells in allogeneic stem cell transplantation. Blood 2011; 118: E82-e92.
45. Venken K, Thewissen M, Hellings N, Somers V, Hensen K, Rummens JL et al. A CFSE based assay for measuring CD4CD25 regulatory T cell mediated suppression of auto-antigen specific and polyclonal T cell responses. J Immunol Methods 2007; 322: 1-11.