Differential expression of CD97 on human lymphocyte subsets and limited effect of CD97 antibodies on allogeneic T-cell stimulation

Immunology Letters

Volumn 123, Issue 2, 2009, Pages 160-168

  Kop, Else N ^a   Matmati, Mourad ^a,b   Pouwels, Walter ^a   Leclercq, Georges ^b   Tak, Paul P ^a   Hamann, Jörg ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

EGF TM7 family; Expression analysis; Human; Lymphocyte subsets; Mixed lymphocyte culture

Indexed keywords

CD97 ANTIGEN; CD97 MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ARTICLE; B LYMPHOCYTE; CELL DEGENERATION; CELL MATURATION; CELL MEMBRANE PERMEABILITY; CELL MOTION; CELL PROLIFERATION; CELL STIMULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG MECHANISM; EFFECTOR CELL; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN TISSUE; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE SUBPOPULATION; LYMPHOID TISSUE; MEMORY CELL; MIXED CELL CULTURE; MIXED LYMPHOCYTE CULTURE; NATURAL KILLER CELL; PRIORITY JOURNAL; STEM CELL; T LYMPHOCYTE; UPREGULATION;

ANTIBODIES; ANTIGENS, CD; ANTIGENS, CD28; ANTIGENS, CD3; HUMANS; INTERLEUKIN-15; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES; UP-REGULATION;

EID: 67349239894     PISSN: 01652478     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imlet.2009.03.009     Document Type: Article

References (54)

1. Eichler W., Aust G., and Hamann D. Characterization of an early activation-dependent antigen on lymphocytes defined by the monoclonal antibody BL-Ac(F2). Scand J Immunol 39 (1994) 111-115
2. Hamann J., Eichler W., Hamann D., Kerstens H.M., Poddighe P.J., Hoovers J.M., et al. Expression cloning and chromosomal mapping of the leukocyte activation antigen CD97, a new seven-span transmembrane molecule of the secretion receptor superfamily with an unusual extracellular domain. J Immunol 155 (1995) 1942-1950
3. Gray J.X., Haino M., Roth M.J., Maguire J.E., Jensen P.N., Yarme A., et al. CD97 is a processed, seven-transmembrane, heterodimeric receptor associated with inflammation. J Immunol 157 (1996) 5438-5447
4. Kwakkenbos M.J., Kop E.N., Stacey M., Matmati M., Gordon S., Lin H.H., et al. The EGF-TM7 family: a postgenomic view. Immunogenetics 55 (2004) 655-666
5. Baud V., Chissoe S.L., Viegas-Pequignot E., Diriong S., N'Guyen V.C., Roe B.A., et al. EMR1, an unusual member in the family of hormone receptors with seven transmembrane segments. Genomics 26 (1995) 334-344
6. Lin H.H., Stacey M., Hamann J., Gordon S., and McKnight A.J. Human EMR2, a novel EGF-TM7 molecule on chromosome 19p13.1, is closely related to CD97. Genomics 67 (2000) 188-200
7. Stacey M., Lin H.H., Hilyard K.L., Gordon S., and McKnight A.J. Human epidermal growth factor (EGF) module-containing mucin-like hormone receptor 3 is a new member of the EGF-TM7 family that recognizes a ligand on human macrophages and activated neutrophils. J Biol Chem 276 (2001) 18863-18870
8. Caminschi I., Lucas K.M., O'Keeffe M.A., Hochrein H., Laabi Y., Köntgen F., et al. Molecular cloning of F4/80-like-receptor, a seven-span membrane protein expressed differentially by dendritic cell and monocyte-macrophage subpopulations. J Immunol 167 (2001) 3570-3576
9. Lin H.H., Chang G.W., Davies J.Q., Stacey M., Harris J., and Gordon S. Autocatalytic cleavage of the EMR2 receptor occurs at a conserved G protein-coupled receptor proteolytic site motif. J Biol Chem 279 (2004) 31823-31832
10. Hamann J., Vogel B., van Schijndel G.M.W., and van Lier R.A.W. The seven-span transmembrane receptor CD97 has a cellular ligand (CD55, DAF). J Exp Med 184 (1996) 1185-1189
11. Hamann J., Stortelers C., Kiss-Toth E., Vogel B., Eichler W., and van Lier R.A.W. Characterization of the CD55 (DAF)-binding site on the seven-span transmembrane receptor CD97. Eur J Immunol 28 (1998) 1701-1707
12. Lin H.H., Stacey M., Saxby C., Knott V., Chaudhry Y., Evans D., et al. Molecular analysis of the epidermal growth factor-like short consensus repeat domain-mediated protein-protein interactions: dissection of the CD97-CD55 complex. J Biol Chem 276 (2001) 24160-24169
13. Stacey M., Chang G.W., Davies J.Q., Kwakkenbos M.J., Sanderson R., Hamann J., et al. The epidermal growth factor-like domains of human EMR2 receptor mediate cell attachment through chondroitin sulphate glycosaminoglycans. Blood 102 (2003) 2916-2924
14. Kwakkenbos M.J., Pouwels W., Matmati M., Stacey M., Lin H.H., Gordon S., et al. Expression of the largest CD97 and EMR2 isoforms on leukocytes facilitates a specific interaction with chondroitin sulfate on B cells. J Leukoc Biol 77 (2005) 112-119
15. Kop E.N., Kwakkenbos M.J., Teske G.J.D., Kraan M.C., Smeets T.J., Stacey M., et al. Identification of the epidermal growth factor-TM7 receptor EMR2 and its ligand dermatan sulfate in rheumatoid synovial tissue. Arthritis Rheum 52 (2005) 442-450
16. Wang T., Ward Y., Tian L.H., Lake R., Guedez L., Stetler-Stevenson W.G., et al. CD97, an adhesion receptor on inflammatory cells, stimulates angiogenesis through binding integrin counterreceptors on endothelial cells. Blood 105 (2005) 2836-2844
17. Eichler W., Hamann J., and Aust G. Expression characteristics of the human CD97 antigen. Tissue Antigens 50 (1997) 429-438
18. Jaspars L.H., Vos W., Aust G., van Lier R.A.W., and Hamann J. Tissue distribution of the human CD97 EGF-TM7 receptor. Tissue Antigens 57 (2001) 325-331
19. Aust G., Eichler W., Laue S., Lehmann I., Heldin N.E., Lotz O., et al. CD97: a dedifferentiation marker in human thyroid carcinomas. Cancer Res 57 (1997) 1798-1806
20. Aust G., Steinert M., Schütz A., Wahlbuhl M., Hamann J., and Wobus M. CD97, but not its closely related EGF-TM7 family member EMR2, is expressed on gastric, pancreatic, and esophageal carcinomas. Am J Clin Pathol 118 (2002) 699-707
21. Aust G., Wandel E., Boltze C., Sittig D., Schütz A., Horn L.C., et al. Diversity of CD97 in smooth muscle cells. Cell Tissue Res 324 (2006) 139-147
22. Wang T., Tian L., Haino M., Gao J.L., Lake R., Ward Y., et al. Improved antibacterial host defense and altered peripheral granulocyte homeostasis in mice lacking the adhesion class G protein receptor CD97. Infect Immun 75 (2007) 1144-1153
23. Veninga H., Becker S., Hoek R.M., Wobus M., Wandel E., van der Kaa J., et al. Analysis of CD97 expression and manipulation: antibody treatment but not gene targeting curtails granulocyte migration. J Immunol 181 (2008) 6574-6583
24. Leemans J.C., te Velde A.A., Florquin S., Bennink R.J., de Bruin K., van Lier R.A.W., et al. The epidermal growth factor-seven transmembrane (EGF-TM7) receptor CD97 is required for neutrophil migration and host defense. J Immunol 172 (2004) 1125-1131
25. Kop E.N., Adriaansen J., Smeets T.J., Vervoordeldonk M.J., van Lier R.A., Hamann J., et al. CD97 neutralisation increases resistance to collagen-induced arthritis in mice. Arthritis Res Ther 8 (2006) R155
26. Van P.M., Hagoort H., Kwakkenbos M.J., Hamann J., and Fibbe W.E. Differential role of CD97 in interleukin-8-induced and granulocyte-colony stimulating factor-induced hematopoietic stem and progenitor cell mobilization. Haematologica 93 (2008) 601-604
27. Capasso M., Durrant L.G., Stacey M., Gordon S., Ramage J., and Spendlove I. Costimulation via CD55 on human CD4+ T cells mediated by CD97. J Immunol 177 (2006) 1070-1077
28. Abbott R.J., Spendlove I., Roversi P., Fitzgibbon H., Knott V., Teriete P., et al. Structural and functional characterization of a novel T cell receptor co-regulatory protein complex, CD97-CD55. J Biol Chem 282 (2007) 22023-22032
29. Van Lier R.A., Boot J.H., Verhoeven A.J., de Groot E.R., Brouwer M., and Aarden L.A. Functional studies with anti-CD3 heavy chain isotype switch-variant monoclonal antibodies. Accessory cell-independent induction of interleukin 2 responsiveness in T cells by epsilon-anti-CD3. J Immunol 139 (1987) 2873-2879
30. De Jong R., Stokkers P., Lamme E., Kool J.M., Borst F., Brouwer M., et al. Regulation of T-cell differentiation by CD2 and CD28 accessory molecules. Immunology 74 (1991) 175-182
31. Rentenaar R.J., Vosters J.L., van Diepen F.N., Remmerswaal E.B., van Lier R.A., and ten Berge I. Differentiation of human alloreactive CD8(+) T cells in vitro. Immunology 105 (2002) 278-285
32. Song H.K., Noorchashm H., Lieu Y.K., Rostami S., Greeley S.A., Barker C.F., et al. Cutting edge: Alloimmune responses against major and minor histocompatibility antigens: distinct division kinetics and requirement for CD28 costimulation. J Immunol 162 (1999) 2467-2471
33. Kwakkenbos M.J., Chang G.W., Lin H.H., Pouwels W., de Jong E.C., van Lier R.A.W., et al. The human EGF-TM7 family member EMR2 is a heterodimeric receptor expressed on myeloid cells. J Leukoc Biol 71 (2002) 854-862
34. Klein U., Rajewsky K., and Küppers R. Human immunoglobulin (Ig)M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J Exp Med 188 (1998) 1679-1689
35. Bohnhorst J.O., Bjorgan M.B., Thoen J.E., Natvig J.B., and Thompson K.M. Bm1-Bm5 classification of peripheral blood B cells reveals circulating germinal center founder cells in healthy individuals and disturbance in the B cell subpopulations in patients with primary Sjogren's syndrome. J Immunol 167 (2001) 3610-3618
36. Hamann D., Baars P.A., Hooibrink B., and van Lier R.W. Heterogeneity of the human CD4+ T-cell population: two distinct CD4+ T-cell subsets characterized by coexpression of CD45RA and CD45RO isoforms. Blood 88 (1996) 3513-3521
37. Hamann D., Baars P.A., Rep M.H., Hooibrink B., Kerkhof-Garde S.R., Klein M.R., et al. Phenotypic and functional separation of memory and effector human CD8+ T cells. J Exp Med 186 (1997) 1407-1418
38. Appay V., van Lier R.A., Sallusto F., and Roederer M. Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 73 (2008) 975-983
39. Cooper M.A., Fehniger T.A., Turner S.C., Chen K.S., Ghaheri B.A., Ghayur T., et al. Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood 97 (2001) 3146-3151
40. Cooper M.A., Fehniger T.A., and Caligiuri M.A. The biology of human natural killer-cell subsets. Trends Immunol 22 (2001) 633-640
41. Nikolaeva N., Uss E., van Leeuwen E.M., van Lier R.A., and ten Berge I. Differentiation of human alloreactive CD4+ and CD8+ T cells in vitro. Transplantation 78 (2004) 815-824
42. Barreiro O., de la Fuente H., Mittelbrunn M., and Sanchez-Madrid F. Functional insights on the polarized redistribution of leukocyte integrins and their ligands during leukocyte migration and immune interactions. Immunol Rev 218 (2007) 147-164
43. Uss E., Rowshani A.T., Hooibrink B., Lardy N.M., van Lier R.A., and ten Berge I. CD103 is a marker for alloantigen-induced regulatory CD8+ T cells. J Immunol 177 (2006) 2775-2783
44. Pickl W.E., Majdic O., Mai I., Gadd S., and Knapp W. Overview of CD97. In: Schlossman S.F., Boumsell L., Gilks W., Harlan J.M., Kishimoto T., Morimoto C., et al. (Eds). Leucocyte Typing V (1995), Oxford University Press, Oxford 1151-1153
45. Eichler W. CD97 isoform expression in leukocytes. J Leukoc Biol 68 (2000) 561-567
46. Kwakkenbos M.J., Matmati M., Madsen O., Pouwels W., Wang Y., Bontrop R.E., et al. An unusual mode of concerted evolution of the EGF-TM7 receptor chimera EMR2. FASEB J 20 (2006) 2582-2584
47. Wobus M., Vogel B., Schmucking E., Hamann J., and Aust G. N-glycosylation of CD97 within the EGF domains is crucial for epitope accessibility in normal and malignant cells as well as CD55 ligand binding. Int J Cancer 112 (2004) 815-822
48. Shimizu Y., van Seventer G.A., Horgan K.J., and Shaw S. Roles of adhesion molecules in T-cell recognition: fundamental similarities between four integrins on resting human T cells (LFA-1, VLA-4, VLA-5, VLA-6) in expression, binding, and costimulation. Immunol Rev 114 (1990) 109-143
49. Hemler M.E. VLA proteins in the integrin family: structures, functions, and their role on leukocytes. Annu Rev Immunol 8 (1990) 365-400
50. Lublin D.M., and Atkinson J.P. Decay-accelerating factor: biochemistry, molecular biology, and function. Annu Rev Immunol 7 (1989) 35-58
51. Heeger P.S., Lalli P.N., Lin F., Valujskikh A., Liu J., Muqim N., et al. Decay-accelerating factor modulates induction of T cell immunity. J Exp Med 201 (2005) 1523-1530
52. Liu J., Miwa T., Hilliard B., Chen Y., Lambris J.D., Wells A.D., et al. The complement inhibitory protein DAF (CD55) suppresses T cell immunity in vivo. J Exp Med 201 (2005) 567-577
53. Strainic M.G., Liu J., Huang D., An F., Lalli P.N., Muqim N., et al. Locally produced complement fragments C5a and C3a provide both costimulatory and survival signals to naive CD4+ T cells. Immunity 28 (2008) 425-435
54. Yona S., Lin H.H., Dri P., Davies J.Q., Hayhoe R.P., Lewis S.M., et al. Ligation of the adhesion-GPCR EMR2 regulates human neutrophil function. FASEB J 22 (2008) 741-751