Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Cell Types and Lineages in Taste Buds
Rocky Mountain Taste and Smell Center, Department of Cell and Developmental Biology, University of Colorado Health Sciences Center, Denver, CO 80262 USA
Correspondence should be sent to: Thomas E. Finger, e-mail: tom.finger{at}uchsc.edu
Key words: chimera, G protein, NCAM, neurotrophin, receptor, serotonin
Taste buds are the sensory endorgans for gustation. In mammals, taste buds
comprise a collection of ~50–100 elongate epithelial cells and a small number of
proliferative basal cells. Ultrastructural studies reveal three distinct anatomical types
of elongate taste cells within each taste bud: Type I, Type II and Type III, first
defined by Murray based on his studies of rabbit foliate taste buds (Murray, 1973
). Figure
1 summarizes the key features of each
cell type including differences in apical structure, cytoplasmic organelles and nuclear
configuration as well as the overall shape of the taste cell.
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Type I cells, sometimes called ‘dark cells’ (e.g. Delay et al., 1986
;
Nelson and Finger, 1993;
Pumplin et al., 1997) extend
lamellate processes around other types of taste cells and express GLAST, a glial
glutamate transporter (Lawton et al.,
2000). These features suggest a glial function for Type I cells, e.g.
transmitter clearance and functional isolation of other taste cell types.
Type II taste cells have a characteristic large, round nucleus and express all of the
elements of the taste transduction cascade for sweet, umami and bitter, including T1R or
T2R families of taste receptors (for bitter, sweet and umami) (Hoon et al., 1999;
Miyoshi et al., 2001), the
downstream transduction components, PLCß2 and IP3R3 (Clapp et al., 2001;
Miyoshi et al., 2001), and
gustducin (Boughter et al.,
1997;
Yang et al., 2000b). These
taste cells thus are the transducing cells for these taste qualities.
Type III cells are characterized by morphologically identifiable synaptic contacts
with the gustatory nerve fibers and expression of the synaptic membrane protein
(Yang et al., 2000a) SNAP25
as well as the neural cell adhesion molecule (NCAM) (Nelson and Finger, 1993). The presence of a prominent
synaptic contact implicates these cells in transmission of information to the nervous
system.
A continuing question in the field is how the different types of elongate taste cells
come to be replaced from the proliferative basal cell population. Two main hypotheses
have been put forward: (i) that the different cell types arise from a common progenitor
which generates a single type of cell which then morphs from one cell type to another as
it matures; and (ii) that a basal cell gives rise to an immature taste cell which then
differentiates into only one of the different morphological types of taste cell. The most
recent postulation of the single lineage hypothesis suggested that Type I cells change
into Type III cells which then mature into Type II cells (Delay et al., 1986). However, our recent studies
entailing chimeric analysis in mice (Stone et
al., 2002) demonstrate that multiple lineages must exist within a taste
bud, i.e that the three cell types are not merely different stages of development of a
single taste cell type.
Recent data from Miura and co-workers (Kusakabe et al., 2002;
Miura et al., 2003; see also
Miura, these proceedings) suggest that Type II and Type III cells may originate from a
common cell, one that expresses NCAM and Mash1. We re-evaluated our chimeric analysis
data to test the possibility that Type I cells may originate from one basal cell
population while Type II and III cells derive from a separate proliferative population.
In order to perform this re-analysis, we made the assumption that Type I cells represent
roughly 40% of the population of cells in any given taste buds. Accordingly we
reduced by 40% the total number of cells for each counted taste bud in the
previous study. Recognizing that this is a crude approximation at best, we still were
able to test the question of whether serotonin-expressing taste cells (a subset of Type
III cells) tend to carry the chimeric marker at higher than a chance rate, i.e. whether
Type III cells still represent a distinct lineage after mathematically eliminating the
Type I cells. None of the taste buds examined in the previous study show a significant
correlation of chimeric marker and serotonergic phenotype after elimination of the
presumed Type I cells (40% of the total population). Hence we have no evidence for
a distinct serotonin lineage once we assume that Type I cells arise from a different
proliferative population. It is important to note that this re-analysis does not prove
that Type II and Type III cells arise from a common progenitor, rather the analysis says
that we have insufficient data to disprove the hypothesis of common lineage. Thus the
question of whether Type II and Type III cells are distinct lineages or merely different
endpoints from a common intermediate cell type remains open to further investigation.
In summary, taking together the morphological, molecular and lineage studies, two
likely hypotheses emerge as to lineage within taste buds. One possibility is that the
three different cell types: Type I, Type II and Type III each arise from a unique
proliferative population, whether it be a progenitor cell population or merely an
intermediate transit amplifying population. Alternatively, there may exist two
proliferative populations, one that generates only Type I cells and the other which
generates an immature cell which can differentiate into either a Type II cell or a Type
III cell. We consider it highly unlikely that a mature Type III cell morphs into a
phenotypically mature Type II cell. Several features mitigate against this scheme. First,
in transgenic mice wherein ß-gal is driven from the BDNF locus (Yee et al., 2003), phenotypically mature Type III
cells express the ß-gal protein which is stable for several days even in the absence
of protein synthesis. Based on BrDU birth-dating studies, we know that both Type II and
Type III cells reach phenotypic maturity at 3–4 days post-mitosis (see
Boughter et al., 1997;
Yee et al., 2003). If Type
III cells regularly transform into Type II cells over a 24 h period, then we would expect
to find numerous Type II cells retaining high levels of ß-gal protein. Only rare Type
II cells show coincident ß-gal label. Further, transformation of a Type III cell into
a Type II cell would necessitate major re-organization of the apical cytoskeleton and
loss of synaptic structures, all in the same 24 h. period. While these considerations do
not totally exclude the possibility of Type III cells transforming into Type II cells, we
believe that other hypotheses are more parsimonious.
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References |
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