Home LiteratureArticle Details
PMID: 8636222 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Visualization of CD2 interaction with LFA-3 and determination of the two-dimensional dissociation constant for adhesion receptors in a contact area.

The Journal of cell biology ·Vol. 132 ·No. 3 ·1996-02-00 ·Pages 465-74

Dustin ML, Ferguson LM, Chan PY, Springer TA, Golan DE

Abstract

Many adhesion receptors have high three-dimensional dissociation constants (Kd) for counter-receptors compared to the KdS of receptors for soluble extracellular ligands such as cytokines and hormones. Interaction of the T lymphocyte adhesion receptor CD2 with its counter-receptor, LFA-3, has a high solution-phase Kd (16 microM at 37 degrees C), yet the CD2/LFA-3 interaction serves as an effective adhesion mechanism. We have studied the interaction of CD2 with LFA-3 in the contact area between Jurkat T lymphoblasts and planar phospholipid bilayers containing purified, fluorescently labeled LFA-3. Redistribution and lateral mobility of LFA-3 were measured in contact areas as functions of the initial LFA-3 surface density and of time after contact of the cells with the bilayers. LFA-3 accumulated at sites of contact with a half-time of approximately 15 min, consistent with the previously determined kinetics of adhesion strengthening. The two-dimensional Kd for the CD2/LFA-3 interaction was 21 molecules/microns 2, which is lower than the surface densities of CD2 on T cells and LFA-3 on most target or stimulator cells. Thus, formation of CD2/LFA-3 complexes should be highly favored in physiological interactions. Comparison of the two-dimensional (membrane-bound) and three-dimensional (solution-phase) KdS suggest that cell-cell contact favors CD2/LFA-3 interaction to a greater extent than that predicted by the three-dimensional Kd and the intermembrane distance at the site of contact. LFA-3 molecules in the contact site were capable of lateral diffusion in the plane of the phospholipid bilayer and did not appear to be irreversibly trapped in the contact area, consistent with a rapid off-rate. These data provide insights into the function of low affinity interactions in adhesion.

MeSH Terms
Antibodies, Monoclonal Binding Sites CD2 Antigens/physiology CD58 Antigens/physiology Cell Adhesion Cell Line Humans Intercellular Junctions/physiology,ultrastructure Kinetics Lipid Bilayers Liposomes Lymphoma, T-Cell Tumor Cells, Cultured
Chemicals
Antibodies, Monoclonal CD2 Antigens CD58 Antigens Lipid Bilayers Liposomes
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Dustin M L
Center for Immunology, Washington University School of Medicine, St. Louis, Missouri 63110, USA.
Ferguson L M
Chan P Y
Springer T A
Golan D E
References (45)
45 references, click to expand
  1. Adhesion receptors of the immune system.
    Nature. 1990 Aug 2;346(6283):425-34 PMID: 1974032
  2. Structure, expression, and genetic linkage of the mouse BCM1 (OX45 or Blast-1) antigen. Evidence for genetic duplication giving rise to the BCM1 region on mouse chromosome 1 and the CD2/LFA3 region on mouse chromosome 3.
    J Exp Med. 1990 Jun 1;171(6):2115-30 PMID: 1693656
  3. Complementary roles for CD2 and LFA-1 adhesion pathways during T cell activation.
    Eur J Immunol. 1991 Mar;21(3):605-10 PMID: 1672642
  4. Role of lymphocyte adhesion receptors in transient interactions and cell locomotion.
    Annu Rev Immunol. 1991;9:27-66 PMID: 1716919
  5. Influence of receptor lateral mobility on adhesion strengthening between membranes containing LFA-3 and CD2.
    J Cell Biol. 1991 Oct;115(1):245-55 PMID: 1717480
  6. Intercellular adhesion molecule 3, a third adhesion counter-receptor for lymphocyte function-associated molecule 1 on resting lymphocytes.
    J Exp Med. 1992 Jan 1;175(1):185-90 PMID: 1730916
  7. Regulation of locomotion and cell-cell contact area by the LFA-1 and ICAM-1 adhesion receptors.
    J Immunol. 1992 May 1;148(9):2654-63 PMID: 1349320
  8. Crystal structure at 2.8 A resolution of a soluble form of the cell adhesion molecule CD2.
    Nature. 1992 Nov 19;360(6401):232-9 PMID: 1279440
  9. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1.
    Nature. 1993 Jul 1;364(6432):33-9 PMID: 8316295
  10. Mutational analysis of the CD2/CD58 interaction: the binding site for CD58 lies on one face of the first domain of human CD2.
    J Exp Med. 1993 Aug 1;178(2):549-58 PMID: 7688025
  11. The CD58 (LFA-3) binding site is a localized and highly charged surface area on the AGFCC'C" face of the human CD2 adhesion domain.
    Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11613-7 PMID: 7505442
  12. Expression cloning of an equine T-lymphocyte glycoprotein CD2 cDNA. Structure-based analysis of conserved sequence elements.
    Eur J Biochem. 1994 Feb 1;219(3):969-76 PMID: 7906650
  13. Human cell-adhesion molecule CD2 binds CD58 (LFA-3) with a very low affinity and an extremely fast dissociation rate but does not bind CD48 or CD59.
    Biochemistry. 1994 Aug 23;33(33):10149-60 PMID: 7520278
  14. The protein tyrosine kinase p56lck regulates cell adhesion mediated by CD4 and major histocompatibility complex class II proteins.
    J Exp Med. 1994 Nov 1;180(5):1729-39 PMID: 7964457
  15. Transient intercellular adhesion: the importance of weak protein-protein interactions.
    Trends Biochem Sci. 1994 Sep;19(9):354-8 PMID: 7985226
  16. Ligand binding by the immunoglobulin superfamily recognition molecule CD2 is glycosylation-independent.
    J Biol Chem. 1995 Jan 6;270(1):369-75 PMID: 7529232
  17. CD8 modulation of T-cell antigen receptor-ligand interactions on living cytotoxic T lymphocytes.
    Nature. 1995 Jan 26;373(6512):353-6 PMID: 7830771
  18. Kinetics of cell detachment: peeling of discrete receptor clusters.
    Biophys J. 1994 Dec;67(6):2522-34 PMID: 7696491
  19. Intracellular mediators regulate CD2 lateral diffusion and cytoplasmic Ca2+ mobilization upon CD2-mediated T cell activation.
    Biophys J. 1995 Feb;68(2):459-70 PMID: 7696499
  20. Topology of the CD2-CD48 cell-adhesion molecule complex: implications for antigen recognition by T cells.
    Curr Biol. 1995 Jan 1;5(1):74-84 PMID: 7697352
  21. Identification and functional characterization of two distinct epitopes on the human T cell surface protein Tp50.
    J Immunol. 1983 Jul;131(1):180-5 PMID: 6190907
  22. Cell adhesion. Competition between nonspecific repulsion and specific bonding.
    Biophys J. 1984 Jun;45(6):1051-64 PMID: 6743742
  23. Allogeneic stimulation of cytotoxic T cells by supported planar membranes.
    Proc Natl Acad Sci U S A. 1984 Oct;81(19):6159-63 PMID: 6333027
  24. Mobility measurement by analysis of fluorescence photobleaching recovery kinetics.
    Biophys J. 1976 Sep;16(9):1055-69 PMID: 786399
  25. Models for the specific adhesion of cells to cells.
    Science. 1978 May 12;200(4342):618-27 PMID: 347575
  26. Phospholipid vesicle formation and transmembrane protein incorporation using octyl glucoside.
    Biochemistry. 1981 Feb 17;20(4):833-40 PMID: 7213617
  27. Stimulation of fluorescence in a small contact region between rat basophil leukemia cells and planar lipid membrane targets by coherent evanescent radiation.
    J Biol Chem. 1982 Jun 10;257(11):6440-5 PMID: 6804467
  28. Three distinct antigens associated with human T-lymphocyte-mediated cytolysis: LFA-1, LFA-2, and LFA-3.
    Proc Natl Acad Sci U S A. 1982 Dec;79(23):7489-93 PMID: 6984191
  29. Development of cell surface linkage complexes in cultured fibroblasts.
    J Cell Biol. 1985 Apr;100(4):1103-14 PMID: 3884631
  30. Distribution of the cell substratum attachment (CSAT) antigen on myogenic and fibroblastic cells in culture.
    J Cell Biol. 1985 May;100(5):1528-39 PMID: 3921554
  31. Purification and characterization of the lymphocyte function-associated-2 (LFA-2) molecule.
    J Immunol. 1986 Jun 1;136(11):4181-7 PMID: 3517166
  32. Supported planar membranes in studies of cell-cell recognition in the immune system.
    Biochim Biophys Acta. 1986 Jun 12;864(1):95-106 PMID: 2941079
  33. Purified lymphocyte function-associated antigen 3 binds to CD2 and mediates T lymphocyte adhesion.
    J Exp Med. 1987 Mar 1;165(3):677-92 PMID: 3102676
  34. The T lymphocyte glycoprotein CD2 binds the cell surface ligand LFA-3.
    Nature. 1987 Mar 26-Apr 1;326(6111):400-3 PMID: 2951597
  35. Structure of the human class I histocompatibility antigen, HLA-A2.
    Nature. 1987 Oct 8-14;329(6139):506-12 PMID: 3309677
  36. Direct evidence for a receptor-ligand interaction between the T-cell surface antigen CD2 and lymphocyte-function-associated antigen 3.
    Proc Natl Acad Sci U S A. 1987 Oct;84(19):6864-8 PMID: 3309949
  37. An LFA-3 cDNA encodes a phospholipid-linked membrane protein homologous to its receptor CD2.
    Nature. 1987 Oct 29-Nov 4;329(6142):840-2 PMID: 3313052
  38. Monoclonal antibody and ligand binding sites of the T cell erythrocyte receptor (CD2).
    Nature. 1987 Oct 29-Nov 4;329(6142):842-6 PMID: 2444890
  39. Interaction between CD4 and class II MHC molecules mediates cell adhesion.
    Nature. 1987 Nov 19-25;330(6145):256-9 PMID: 2823150
  40. The immunoglobulin superfamily--domains for cell surface recognition.
    Annu Rev Immunol. 1988;6:381-405 PMID: 3289571
  41. T-cell antigen receptor genes and T-cell recognition.
    Nature. 1988 Aug 4;334(6181):395-402 PMID: 3043226
  42. Interpretation of fluorescence correlation spectroscopy and photobleaching recovery in terms of molecular interactions.
    Methods Cell Biol. 1989;30:307-32 PMID: 2648114
  43. Ligand interactions of the cation-independent mannose 6-phosphate receptor. The stoichiometry of mannose 6-phosphate binding.
    J Biol Chem. 1989 May 15;264(14):7962-9 PMID: 2542254
  44. The specific interaction of helper T cells and antigen-presenting B cells. IV. Membrane and cytoskeletal reorganizations in the bound T cell as a function of antigen dose.
    J Exp Med. 1989 Nov 1;170(5):1697-713 PMID: 2530300
  45. Cytoskeletal function in CD8- and T cell receptor-mediated interaction of cytotoxic T lymphocytes with class I protein.
    J Exp Med. 1991 Jan 1;173(1):241-9 PMID: 1898662
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1996-02-00
Pages
465-74
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120727
Subset
IM
Grants
NCI NIH HHS · CA31798 · United States
NHLBI NIH HHS · HL15157 · United States
NHLBI NIH HHS · HL32854 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com