Sialyl Lewis x (CD15s) identifies highly differentiated and most suppressive FOXP3high regulatory T cells in humans

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 23, 2015, Pages 7225-7230

  Miyara, Makoto ^a,b   Chader, Driss ^a,b   Sage, Edouard ^c   Sugiyama, Daisuke ^d   Nishikawa, Hiroyoshi ^d   Bouvry, Diane ^e   Claër, Laetitia ^a,b   Hingorani, Ravi ^f   Balderas, Robert ^f   Rohrer, Jurg ^f   Warner, Noel ^f   Chapelier, Alain ^c   Valeyre, Dominique ^e   Kannagi, Reiji ^g   Sakaguchi, Shimon ^d   Amoura, Zahir ^a,b,h   Gorochov, Guy ^a,b,h  

^a Assistance publique Hôpitaux de Paris   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c FOCH HOSPITAL   (France)

^d OSAKA UNIVERSITY   (Japan)

^e AVICENNE HOSPITAL   (France)

^f BD Technologies   (United States)

^g AICHI MEDICAL UNIVERSITY   (Japan)

^h SORBONNE UNIVERSITÉ   (France)

Author keywords

Autoimmunity; CD15s; FOXP3; Regulatory T cells; Tumor immunity

Indexed keywords

CYTOKINE; SIALYL LEWIS X ANTIGEN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TUMOR ANTIGEN; VIRUS ANTIGEN; AUTACOID; CD15 ANTIGEN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; MONOCLONAL ANTIBODY;

ARTICLE; CELL SURFACE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFLAMMATION; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SARCOIDOSIS; T CELL DEPLETION; T LYMPHOCYTE SUBPOPULATION; CYTOLOGY; FLOW CYTOMETRY; IMMUNOLOGY; METABOLISM; SECRETION (PROCESS); THYMUS;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD15; CYTOKINES; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INFLAMMATION MEDIATORS; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND;

EID: 84931291785     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1508224112     Document Type: Article

References (36)

1. Sakaguchi S, Yamaguchi T, Nomura T, Ono M (2008) Regulatory T cells and immune tolerance. Cell 133(5):775-787.
2. Sakaguchi S, Miyara M, Costantino CM, Hafler DA (2010) FOXP3+ regulatory T cells in the human immune system. Nat Rev Immunol 10(7):490-500.
3. Allan SE, et al. (2007) Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production. Int Immunol 19(4):345-354.
4. Miyara M, et al. (2009) Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity 30(6):899-911.
5. Ito T, et al. (2008) Two functional subsets of FOXP3+ regulatory T cells in human thymus and periphery. Immunity 28(6):870-880.
6. Baecher-Allan C, Wolf E, Hafler DA (2006) MHC class II expression identifies functionally distinct human regulatory T cells. J Immunol 176(8):4622-4631.
7. Borsellino G, et al. (2007) Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: Hydrolysis of extracellular ATP and immune suppression. Blood 110(4):1225-1232.
8. Thornton AM, et al. (2010) Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J Immunol 184(7):3433-3441.
9. Deaglio S, et al. (2007) Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 204(6):1257-1265.
10. Fritzsching B, et al. (2005) In contrast to effector T cells, CD4+CD25+FoxP3+ regulatory T cells are highly susceptible to CD95 ligand-but not to TCR-mediated cell death. J Immunol 175(1):32-36.
11. Solstad T, et al. (2011) CD147 (Basigin/Emmprin) identifies FoxP3+CD45RO+CTLA4+- activated human regulatory T cells. Blood 118(19):5141-5151.
12. Liu W, et al. (2006) CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J Exp Med 203(7):1701-1711.
13. Seddiki N, et al. (2006) Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. J Exp Med 203(7):1693-1700.
14. Hoffmann P, et al. (2006) Only the CD45RA+ subpopulation of CD4+CD25high T cells gives rise to homogeneous regulatory T-cell lines upon in vitro expansion. Blood 108(13):4260-4267.
15. Battaglia M, et al. (2006) Rapamycin promotes expansion of functional CD4+CD25+ FOXP3+ regulatory T cells of both healthy subjects and type 1 diabetic patients. J Immunol 177(12):8338-8347.
16. Nunes-Cabaço H, Caramalho I, Sepúlveda N, Sousa AE (2011) Differentiation of human thymic regulatory T cells at the double positive stage. Eur J Immunol 41(12): 3604-3614.
17. Sugiyama D, et al. (2013) Anti-CCR4 mAb selectively depletes effector-type FoxP3+ CD4+ regulatory T cells, evoking antitumor immune responses in humans. Proc Natl Acad Sci USA 110(44):17945-17950.
18. Hallermann C, Niermann C, Schulze HJ (2007) Regulatory T-cell phenotype in association with large cell transformation of mycosis fungoides. Eur J Haematol 78(3): 260-263.
19. Miyara M, Amoura Z, Gorochov G (2009) Human lupus, fewer Treg cells indeed: Comment on the article by Venigalla et al. Arthritis Rheum 60(2):630.
20. Miyara M, et al. (2005) Global natural regulatory T cell depletion in active systemic lupus erythematosus. J Immunol 175(12):8392-8400.
21. Munro JM, et al. (1992) Expression of sialyl-Lewis X, an E-selectin ligand, in inflammation, immune processes, and lymphoid tissues. Am J Pathol 141(6):1397-1408.
22. Easton EW, Schiphorst WE, van Drunen E, van der Schoot CE, van den Eijnden DH (1993) Human myeloid alpha 3-fucosyltransferase is involved in the expression of the sialyl-Lewis(x) determinant, a ligand for E- and P-selectin. Blood 81(11):2978-2986.
23. Sugimoto N, et al. (2006) Foxp3-dependent and -independent molecules specific for CD25+CD4+ natural regulatory T cells revealed by DNA microarray analysis. Int Immunol 18(8):1197-1209.
24. Natsuka S, Gersten KM, Zenita K, Kannagi R, Lowe JB (1994) Molecular cloning of a cDNA encoding a novel human leukocyte alpha-1,3-fucosyltransferase capable of synthesizing the sialyl Lewis x determinant. J Biol Chem 269(24):16789-16794.
25. Sasaki K, et al. (1994) Expression cloning of a novel alpha 1,3-fucosyltransferase that is involved in biosynthesis of the sialyl Lewis x carbohydrate determinants in leukocytes. J Biol Chem 269(20):14730-14737.
26. de Vries T, Knegtel RM, Holmes EH, Macher BA (2001) Fucosyltransferases: Structure/function studies. Glycobiology 11(10):119R-128R.
27. Polley MJ, et al. (1991) CD62 and endothelial cell-leukocyte adhesion molecule 1 (ELAM-1) recognize the same carbohydrate ligand, sialyl-Lewis x. Proc Natl Acad Sci USA 88(14):6224-6228.
28. Siegmund K, et al. (2005) Migration matters: Regulatory T-cell compartmentalization determines suppressive activity in vivo. Blood 106(9):3097-3104.
29. Gottschalk RA, Corse E, Allison JP (2012) Expression of Helios in peripherally induced Foxp3+ regulatory T cells. J Immunol 188(3):976-980.
30. Himmel ME, MacDonald KG, Garcia RV, Steiner TS, Levings MK (2013) Helios+ and Helios-cells coexist within the natural FOXP3+ T regulatory cell subset in humans. J Immunol 190(5):2001-2008.
31. Serre K, et al. (2011) Helios is associated with CD4 T cells differentiating to T helper 2 and follicular helper T cells in vivo independently of Foxp3 expression. PLoS ONE 6(6): e20731.
32. Joller N, et al. (2014) Treg cells expressing the coinhibitory molecule TIGIT selectively inhibit proinflammatory Th1 and Th17 cell responses. Immunity 40(4):569-581.
33. Miyara M, et al. (2006) The immune paradox of sarcoidosis and regulatory T cells. J Exp Med 203(2):359-370.
34. van den Hoogen F, et al. (2013) 2013 classification criteria for systemic sclerosis: An American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis 72(11):1747-1755.
35. Olsen EA, et al.; International Society for Cutaneous Lymphomas; United States Cutaneous Lymphoma Consortium; Cutaneous Lymphoma Task Force of the European Organisation for Research and Treatment of Cancer (2011) Clinical end points and response criteria in mycosis fungoides and Sézary syndrome: A consensus statement of the International Society for Cutaneous Lymphomas, the United States Cutaneous Lymphoma Consortium, and the Cutaneous Lymphoma Task Force of the European Organisation for Research and Treatment of Cancer. J Clin Oncol 29(18):2598-2607.
36. Jaretzki A, 3rd, et al.; Task Force of the Medical Scientific Advisory Board of the Myasthenia Gravis Foundation of America (2000) Myasthenia gravis: Recommendations for clinical research standards. Ann Thorac Surg 70(1):327-334.