[CANCER RESEARCH 48, 37-40, January 1, 1988]
Molecular Pathways of Adhesion in Spontaneous Resetting of T-Lymphocytes to
the Hodgkin's Cell Line L428
Martin E. Sanders,1 M. William Makgoba, Eileen H. Sussman, Gale E. G. Luce, Jeffrey Cossman, and
Stephen Shaw
The Immunology Branch [M. E. S., M. W. M., G. E. G. L., S. SJ and the Laboratory of Pathology [E. H. S., J. C.J, National Cancer Institute, NIH,
Bethesda, Maryland 20892
ABSTRACT
Spontaneous resetting of T-lymphocytes to Reed-Sternberg cells has
been observed both in vitro and in vivo but its molecular mechanism has
not been defined. We have investigated such resetting using the Hodgkin's
cell line L428. L428 expresses high levels of LFA-3 and ICAM-1, both
of which are ligands for T-cell adhesion. Monoclonal antibody inhibition
of spontaneous resetting indicated that it is not dependent on the T-cell
receptor complex but is largely mediated by interaction of T-cell CD2
(Tll/E-rosette receptor) with its ligand LFA-3 on I 428 cells. Studies
using an alternate assay of adhesion (conjugate formation) confirm the
roles of CD2/LFA-3 and also implicate a second mode of binding via
LFA-1 on T-cells to ICAM-1 on L428. These data explain the previously
reported finding of T-cell resetting with Reed-Sternberg cells as an
exaggeration of normal antigen-independent T-cell adhesion.
INTRODUCTION
RS2 cells are a malignant cell type of uncertain origin that
are found in diseased lymphoid tissues of patients with Hodg-
kin's disease. A unique characteristic of RS cells is that they
spontaneously form rosettes with T-lymphocytes (1-3). Such
rosettes form rapidly in vitro with autologous lymphocytes in
single cell suspensions of fresh splenic tissue or lymph nodes
from patients with Hodgkin's disease; rosettes also form with
allogeneic lymphocytes (4). In vivo adhesion of lymphocytes to
RS cells is evidenced by the frequent finding of similar clusters
of lymphocytes around RS cells in Giemsa-stained imprints of
Hodgkin's tissue sections (2), as well as electron microscopic
studies of Hodgkin's tissues showing tight apposition and uro
pod formation between lymphocytes and RS cells (5, 6).
The pathophysiological relevance of such lymphocytes sur
rounding RS cells in tissue sections to tumor immunity has
remained unclear. One study suggested that the finding of large
numbers of autologous lymphocytes adherent to RS cells in
tissue suspension was a favorable prognostic indicator (7).
Furthermore, one electron microscopic study (6) noted ultra-
structural changes in the RS cells suggesting a cytotoxic effect
of the surrounding lymphocytes. However, other studies have
demonstrated that autologous lymphocytes may adhere to RS
cells in culture for up to several wk without leading to cytolysis
(1, 2).
Progress has been made in elucidating the molecular mech
anisms involved in other models of T-cell adhesion. Studies
have shown that cytotoxic T-lymphocytes may adhere to other
cells via antigen-independent mechanisms (8, 9). Since such
adhesion does not involve the specific antigen receptor, cytolysis
does not occur. Two different molecular pathways of antigen-
independent adhesion have been identified (9). The CD2 mol
ecule (also known as Til, LFA-2, or the sheep erythrocyte
Received 6/25/87; revised 9/23/87; accepted 9/28/87.
The costs of publication of this article were defrayed in part by the payment
of page charges. This article must therefore be hereby marked advertisement in
accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
1To whom requests for reprints should be addressed, at NIH, Bldg. 10, Room
4BI7, Bethesda, MD 20892.
2The abbreviations used are: RS, Reed-Sternberg; MAB, monoclonal antibody.
receptor) on T-lymphocytes mediates adhesion via binding to
lymphocyte function-associated antigen 3 (LFA-3), a ubiqui
tously distributed cell surface glycoprotein (10, 11). CD2 bind
ing to LFA-3 is the mechanism of adhesion in the phenomenon
of rosette formation of T-lymphocytes with human erythrocytes
( 12,13) and in human thymocyte adhesion to thymic epithelium
(14). The other molecular pathway of T-cell adhesion involves
interaction of T-cell surface LFA-1 with one or more target cell
surface ligands. Functional evidence indicates that intercellular
adhesion molecule 1 (ICAM-1) is one ligand for LFA-1; in
some experimental systems, LFA-1-dependent adhesion of B-
cells and T-cells can be inhibited by anti-ICAM-13 (15).
L428 is a Hodgkin's cell line which has morphological char
acteristics and cell surface marker patterns identical to those of
freshly obtained RS cells and shows the typical RS cell phenom
enon of spontaneous rosette formation with T-lymphocytes (4,
16, 17). In the present study we demonstrate that the observed
spontaneous adhesion of T-lymphocytes to the Hodgkin's cell
line L428 occurs primarily via binding of T-lymphocyte CD2
to L428 cell LFA-3, with some lesser contribution to this
adhesion by T-cell LFA-1 and L428 cell ICAM-1.
MATERIALS AND METHODS
Cells and Reagents. L428 was kindly provided by Dr. V. Diehl,
University of Cologne, Federal Republic of Germany, and was grown
in RPMI 1640 with 10% fetal calf serum. For rosette assays human T-
lymphocytes were purified from peripheral blood mononuclear cells of
normal donors by resetting with 2-aminoethylisothiouronium bromide
hydrobromide-treated sheep erythrocytes. Conjugate assays were per
formed using a cytotoxic T-lymphocyte clone 8.2 (specific for DPw2
and noncytolytic for L428) (18). Monoclonal antibody TS2/9 to LFA-
3 and RR1/1 to ICAM-1 were kindly provided by Dr. T. Springer
(Dana FärberCancer Institute, Boston, MA), (15, 19). MAB 84H10 to
ICAM-1 was kindly provided by Dr. P. Mannoni (Institute J. Paoli-I.
Calmette, Marseille, France). MAB MHM23, specific for the ß chain
of LFA-1, was kindly provided by Dr. J. Hildreth (The Johns Hopkins
University, Baltimore, MD). Anti-CD2 MAB 95-5-49 was kindly pro
vided by Dr. R. Quiñonesand Dr. R. Gress (National Cancer Institute,
NIH, Bethesda, MD). MAB W6/32, to a framework epitope of human
class I HLA, was kindly provided by Dr. S. Jacobson (National Institute
of Neurological and Communicative Disorders and Stroke, NIH, Be
thesda, MD). The CD3 MAB OKT3 was kindly provided by Dr. G.
Goldstein (Ortho Pharmaceuticals, Raritan, NJ). All MABs were used
as purified immunoglobulin. Fab fragments for MAB to LFA-1 and
LFA-3 were prepared by papain digestion.
Flow Microfluorometry. One x 10' cells per sample were incubated
with saturating amounts of relevant antibody or culture supernatant for
30 min at 4°C.After two washes, cells were further incubated with a
saturating amount of goat anti-mouse IgG F(ab')z for 30 min at 4'C.
Following two final washes, 50,000 cells were analyzed on a Becton
Dickinson FACS II flow cytometer and results expressed as linear unit
millivolts.
Rosette Assay. One x IO6 L428 cells and 10 x 10' T-lymphocytes
were added to test tubes containing 1.0 ml of RPMI 1640 with 10%
fetal calf serum and 10 pg of a purified MAB. Tubes were centrifuged
1 M. W. M. ft al., submitted for publication.
37
Research.
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