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Vesicular transport of histamine in stimulated human basophils
AM Dvorak, DW MacGlashan , ES Morgan and LM Lichtenstein
Department of Pathology, Beth Israel Hospital, Boston, MA 02215, USA.
Human basophils participating in experimentally produced contact allergy
display progressive secretion of electron-dense secretory granule contents
and retention of cytoplasmic granule containers in the absence of entire
granule extrusion, a process termed piecemeal degranulation (PMD) and
postulated to be effected by vesicular transport (Dvorak HF, Dvorak AM:
Clin Hematol 4:651, 1975). Proof of this hypothesis was sought using models
of human basophil-stimulated secretion, partially purified human peripheral
blood basophils, and a morphometric analysis of the fraction of total
cellular cytoplasmic vesicles loaded with histamine, a major
proinflammatory mediator present in basophil secretory granules. The
subcellular localization of histamine was accomplished using a new
ultrastructural enzyme-affinity- gold method based on the affinity of
diamine oxidase for its substrate, histamine (Dvorak et al: J Histochem
Cytochem 41:787, 1993). Two models were selected for a kinetic analysis of
stimulated vesicle transport of histamine based on known biochemical and
ultrastructural characteristics (MacGlashan et al: J Immunol 136:2231,
1986; Warner et al: J Leukoc Biol 45:558, 1989; Dvorak et al: Am J Pathol
141:1309, 1992; Dvorak et al: Lab Invest 64:234, 1991). These models were
selected to include the rapid release reaction stimulated by the bacterial
peptide, FMLP, and the slow release reaction stimulated by the phorbol
diester tumor promoter, TPA. The results of this study showed that the
fraction of histamine-loaded cytoplasmic vesicles (%VG/TV/micron2) in
TPA-stimulated basophils significantly exceeded the fraction in
unstimulated cells, a process that persisted for 45 minutes after TPA
stimulation and was associated with extensive PMD and no morphologic
evidence of recovery. Similarly, the fraction of histamine- loaded
cytoplasmic vesicles after FMLP stimulation significantly exceeded the
fraction in unstimulated cells, a process that persisted for 10 minutes
after FMLP stimulation and was associated with the morphologic continuum of
PMD-->anaphylactic degranulation (characterized by extrusion of
granules)-->recovery, a process largely complete in the 10-minute
samples. These studies establish for the first time that an important
proinflammatory mediator, histamine, traffic from secretory granules to the
extracellular milieu in small cytoplasmic vesicles in stimulated human
basophils. The association of this process with the ultrastructural release
reaction defined as PMD produced primarily by TPA and in part by FMLP
establishes vesicular transport as the mechanism for effecting this type of
regulated secretion. Vesicular transport of histamine was also significant
in the more complex stimulated secretory and recovery model produced by
exposure of human basophils to the bacterial peptide FMLP.
Volume 88,
Issue 11,
pp. 4090-4101,
12/01/1996
Copyright © 1996 by The American Society of Hematology
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