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Vol. 10, Issue 12, 4247-4261, December 1999
Laboratory of Skin Biology, National Institute of Arthritis and
Musculoskeletal and Skin Diseases, National Institutes of Health,
Bethesda, Maryland 20892-2752
The cell envelope (CE) is a specialized structure that is important
for barrier function in terminally differentiated stratified squamous
epithelia. The CE is formed inside the plasma membrane and becomes
insoluble as a result of cross-linking of constituent proteins by
isopeptide bonds formed by transglutaminases. To investigate the
earliest stages of assembly of the CE, we have studied human epidermal
keratinocytes induced to terminally differentiate in submerged liquid
culture as a model system for epithelia in general. CEs were harvested
from 2-, 3-, 5-, or 7-d cultured cells and examined by 1) immunogold
electron microscopy using antibodies to known CE or other junctional
proteins and 2) amino acid sequencing of cross-linked peptides derived
by proteolysis of CEs. Our data document that CE assembly is initiated
along the plasma membrane between desmosomes by head-to-tail and
head-to-head cross-linking of involucrin to itself and to envoplakin
and perhaps periplakin. Essentially only one lysine and two glutamine
residues of involucrin and two glutamines of envoplakin were used
initially. In CEs of 3-d cultured cells, involucrin, envoplakin, and
small proline-rich proteins were physically located at desmosomes and
had become cross-linked to desmoplakin, and in 5-d CEs, these three
proteins had formed a continuous layer extending uniformly along the
cell periphery. By this time >15 residues of involucrin were used for cross-linking. The CEs of 7-d cells contain significant amounts of the
protein loricrin, typically expressed at a later stage of CE assembly.
Together, these data stress the importance of juxtaposition of
membranes, transglutaminases, and involucrin and envoplakin in the
initiation of CE assembly of stratified squamous epithelia.
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