High-resolution surface views of human lymphocytes during capping of
CD4 and HLA antigens as revealed by immunogold fracture-flip
ANTONIO PAVAN, PATKIZIA MANCINI, GIUSEPPE LUCANIA, LUIGI FRATI,
MARIA ROSARIA TORRISI*
Dipartimento di Medicina Sperimentale, Universita di Roma "La Sapienza", 324 Viaie Regina Elena, 00161, Roma, Italy
and PEDRO PINTO da SILVA
Membrane Biology Section/Laboratory of Mathematical Biology, National Cancer Institute-Frederick Cancer Research Facility,
Frederick, Maryland 21701, USA
* Author for correspondence
Summary
The surface ultrastructure of lymphocytes during
capping of two transmembrane proteins is shown. As
seen by fracture-flip the plasma membranes of hu-
man lymphocytes are covered by a high density of
surface particles. Incubation in 30 % glycerol leads to
aggregation of these surface particles. Immunogold
labelling shows that the transmembrane proteins
bearing HLA class I and CD4 antigens are confined to
the particle aggregates. These results indicate that
surface particles revealed by fracture-flip represent
surface protrusions of integral membrane proteins
seen as intramembrane particles in freeze-fractured
lymphocytes.
During capping HLA or CD4 antigens aggregate
into progressively larger patches and, finally, into
single caps. As revealed by fracture-flip the patches/
caps are seen as clearly differentiated raised plat-
forms that are clearly and sharply demarcated rela-
tive to contiguous areas of the surface. In non-
patched (non-capped) regions, the pattern of distri-
bution and apparent density of surface particles
remain unaltered. Immunogold labelling clearly
demarcates patches and caps, and shows that vir-
tually no antigen molecules remain dispersed over
the non-patched (non-capped) regions. Estimates of
the surface density of either HLA or CD4 antigens
over the capped areas point to high planar concen-
trations of the transmembrane proteins that bear
these antigens.
Key words: fteeze-fracture, fracture-flip, lymphocytes.
Introduction
Interest in the phenomenon of capping in lymphocytes
goes beyond the immunological significance of capping.
Few phenomena that can be analyzed ultrastructurally
can so well illustrate dynamic events in biological mem-
branes (Nelson et al. 1983; Bourguignon and Bourguignon,
1984; Turner et al. 1988).
The recent introduction of the fracture-flip method made
it possible to observe high-resolution Pt/C replicas of cell
surfaces (Andersson Foreman and Pinto da Silva, 1988a;
Fujimoto and Pinto da Silva, 1988; Pinto da Silva et al.
1989). In fracture-flip the exoplasmic halves of membranes
are stabilized by, and remain attached to, carbon replicas
of freeze-fractured specimens. Inversion ('flipping*) of
these carbon replicas exposes the actual outer surfaces of
plasma membranes, which are then shadowed by Pt/C
evaporation. The method is simple and can be easily
combined with immunogold labelling to produce images of
the planar distribution of surface antigens and receptors
(Andersson Forsman and Pinto da Silva, 1988a; Pimenta
et al. 1989). Immunogold labelling can be combined with
fracture-flip by labelling the specimens either before
Journal of Cell Science 96, 151-157 (1990)
Printed in Great Britain © The Company of Biologists Limited 1990
(Andersson Foreman and Pinto da Silva, 1988a) or after
freeze-fracture (Pimenta et al. 1989).
In previous papers we used label-fracture (Pinto da
Silva and Kan, 1984; Kan and Pinto da Silva, 1987;
Andersson Foreman and Pinto da Silva, 19886) to address
the dynamics and relationships between intramembrane
particles (revealed by freeze-fracture) and the surface
distribution and redistribution of surface antigens (Pavan
et al. 1989a,6). Here, we use fracture-flip and immunogold
fracture-flip to re-approach the investigation of capping
phenomena from the ultrastructural/cytochemical point
of view.
Materials and methods
Human peripheral lymphocytes were isolated from fresh heparin-
ized blood of healthy donors by Ficoll/Hypaque density gradient
centrifugation, and were washed three times in phosphate-
buffered saline (PBS), pH7.4. The native distribution of HLA
class I and CD4 antigens was assessed by treating lymphocytes
unfixed or chemically fixed (1 % glutaraldehyde in PBS, 1 h, 25 °C)
in anti-HLA A,B,C (class I) monoclonal antibody (1:100, in PBS,
lh, 4°C), (a generous gift from Dr M. C. Mazzilli), or 0KT4
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