J. Cell Sci. 85, 231-244 (1986) 231
Printed in Great Britain © The Company of Biologists Limited 1986
ROLE OF CELL ADHESION IN CONTACT-
DEPENDENT TRANSFER OF A LYSOSOMAL ENZYME
FROM LYMPHOCYTES TO FIBROBLASTS
I. OLSEN
1
, T. OLIVER
2
, H. MUIR
1
, R. SMITH
1
AND T. PARTRIDGE
2
Kennedy Institute of Rheumatology, Bute Gardens, London W6 7DW, UK
^Department of Histopathology and Experimental Pathology, Charing Cross and
Westminster Medical School, Fulham Palace Road, London W6 8RF, UK
SUMMARY
Normal lymphocytes were found to adhere strongly to monolayer cultures of fibroblasts deficient
in the lysosomal enzyme, /J-glucuronidase. During this co-culture, the fibroblasts acquired from
the lymphocytes substantial amounts of this enzyme, which often accumulated at sites of contact
between the two types of cell. Enzyme transfer was prevented by addition to the co-cultures either
of purified lymphocyte plasma membranes or of antibody raised against such plasma membranes,
but it was not inhibited by the addition of antibody raised against lymphocyte-derived /S-glu-
curonidase. An active role for the lymphocyte in this contact-dependent process was suggested
by interference contrast, immunofluorescence and scanning electron-microscopic studies. These
revealed extensive arrays of projections of the lymphocyte that ramified over the fibroblast cell
surface. By transmission electron microscopy, conspicuous clusters of micropinocytotic vesicles
were evident in the cytoplasm of the 'recipient' fibroblasts, subjacent to the surface in regions
closely apposed to adherent lymphocytes. Such high frequencies of these vesicles were restricted to
sites of lymphocyte-fibroblast contact, suggesting that they may play an important part in the
transfer of enzyme between these two types of cell.
INTRODUCTION
A major group of inherited metabolic disorders has been identified as being
associated with deficiencies of specific lysosomal enzymes (Stanbury et al. 1983).
Therapy by replacement of the missing enzyme has been attempted in a number of
ways, and transplantation of bone marrow from normal to enzyme-deficient
individuals has been reported to have sometimes produced clinical improvements
(Hugh-Jones et al. 1984).
Two mechanisms have been described whereby, at least in vitro, cells derived
from individuals with inborn lysosomal storage diseases can acquire the missing
enzymes. One, which is now well characterized (Creek & Sly, 1984), involves
endocytosis, via mannose 6-phosphate receptors located on the cell surface, of 'high
uptake' enzyme forms, which bear mannose 6-phosphate groups and are secreted into
the medium by many types of cell. A second, quite different, mechanism has recently
been described by which certain lysosomal enzymes are transferred to genetically
deficient fibroblasts from normal lymphocytes (Olsen et al. 1983). This transfer is
not inhibited by mannose 6-phosphate and requires cell-to-cell contact (Olsen et al.
Key words: enzyme transfer, cell contacts, lymphocytes.