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MICROSCOPY RESEARCH AND TECHNIQUE 44:293–303 (1999)
Dynamic Control of Reversible Cell Adhesion
and Actin Cytoskeleton in the Mouth of Beroë
SIDNEY L. TAMM*
Biology Department, Boston University, Boston, Massachusetts 02115
KEY WORDS
dynamic tissue adhesion; actin-based appositions; ctenophores
ABSTRACT
Cell-cell adhesion in the various types of intercellular junctions of differentiated
tissues is relatively stable and permanent. In migrating cells of embryos, or in wound closure,
inflammatory responses and tumors of adult tissues, however, bonds between cells are made and
broken and made again, i.e., cell-cell adhesions are transient and reversible. These nonjunctional
contacts lack the organized structure of intercellular junctions, but may initiate their tissue-specific
formation during development.
Investigation of dynamic, nonjunctional cell-cell adhesions has been hampered by the asynchronous and heterogeneous distribution of these transient contacts among groups of moving cells. We
recently discovered a novel system of reversible cell adhesion in a differentiated tissue that
overcomes this difficulty. Here I review our current knowledge of this system, particularly its unique
experimental advantages for investigating the mechanisms and control of dynamic cell adhesion.
Microsc Res Tech 44:293–303, 1999. r 1999 Wiley-Liss, Inc.
THE MOUTH OF BEROË
Ctenophores (comb jellies) of the order Beroida are
voracious predators of other gelatinous marine
zooplankton, especially other kinds of ctenophores.
Beroids in surface waters reach lengths of 30 cm, and
have a large mouth and a voluminous stomach that
occupies most of their miter- or cucumber-shaped body.
Beroë actively seeks prey by swimming mouth forward, propelled by the beating of rows of giant ciliary
comb plates (Fig. 1) (Tamm, 1982). The mouth remains
closed, with the body shape streamlined, until the lips
contact prey. Then the mouth opens suddenly and the
stomach cavity rapidly expands to suck in the prey (Fig.
2) (Horridge, 1965a; Tamm, 1982). Complete engulfment of prey as big as the Beroë takes only a few
seconds (Tamm, 1982; Tamm and Tamm, 1993a), facilitated by activation of tooth-like macrocilia lining the
lips or stomodaeum (Horridge, 1965a; Tamm and Tamm,
1993b). The mouth quickly closes and re-seals after
ingestion, and the bloated Beroë swims slowly away to
digest its meal.
MOUTH CLOSURE
Beroid species with thin flexible body walls, flattened
shape, and wide mouths (B. sp. Gloria, B. forskali, B.
mitrata) keep their mouths closed by adhesion between
paired strips of epithelial cells (Tamm and Tamm,
1991b, 1993a). In B. sp. Gloria (⫽B. ovata, G.R. Harbison, personal communication), the focus of our work,
the epithelial adhesive strips run around the inside of
opposing lips; in B. forskali and B. mitrata, the adhesive strips run longitudinally along the midline of the
stomodaeum (Tamm and Tamm, 1991b). The two different orientations of the adhesive strips are correlated
with different patterns of macrocilia inside the stomodaeum. That the epithelial strips serve as belt-like
tissue fasteners can be easily demonstrated in Mg2⫹anaesthetized animals (which lack muscular and neur 1999 WILEY-LISS, INC.
ral responses) by pulling apart the adherent lips or
stomodaeal walls with forceps (Fig. 3) (Tamm and
Tamm, 1991b).
Sections through closed mouths shows that the singlelayered, flattened stomodaeal epithelium is markedly
thicker in the adhesive strips, due to increased height
(20–25 µm) of cells in this region (Fig. 4). The adhesive
strips are about 200 µm wide, and consist of more than
a hundred thousand cells per lip.
The adherent epithelial cells of apposing lips are
joined together by numerous close contacts between
their surface membranes (Figs. 4–6). At these appositions, the plasma membranes of adjoining cells are
highly folded and interdigitated, and run parallel with
a uniform separation of approximately 15 nm (Fig. 6;
Tamm and Tamm, 1991b). The intercellular space often
contains dense flocculent material which sometimes
appears periodically disposed (Fig. 6A,C). The apposed
plasma membranes are lined by a dense cytoplasmic
coat, 15–30 nm thick, which contains numerous 6–8 nm
diameter microfilaments (Fig. 6C,D) (Tamm and Tamm,
1991b; 1993a). Rhodamine phalloidin fluorescence confirms that the dense cytoplasmic coat contains F-actin
(Fig. 7A) (Tamm and Tamm, 1993a).
The regions of close contact alternate with vacuolar
intercellular spaces lacking filamentous membrane coats
(Figs. 4, 5, 6A). A possible reason for these interruptions of
the adhesive contacts will be discussed later.
The two adherent epithelial strips thus appear structurally identical, and have a mirror-image symmetry
about the plane of contact. Apposing strips appear to be
functionally alike as well, and probably make equal
Contract grant sponsor: NIH; contract grant number GM 45557.
*Correspondence to: Sidney L. Tamm, Biology Department, Boston University,
Boston, MA 02215 USA E-mail: tamm@bio.bu.edu
Received 17 March 1998; revision accepted 20 July 1998
294
S.L. TAMM
Fig. 1. Beroë mitrata swimming mouth forward (to the left) with
the lips closed into a wide curved slit. The body is flattened in the
stomodaeal plane with a blunt front end and tapering rear. Longitudinal rows of ciliary comb plates propel the animal forward. Photograph
by Dr. Claude Carré, Station Zoologique, Villefranche-sur-Mer, France.
Natural size. Reprinted from Tamm SL and Tamm S. 199b. Reversible
epithelial adhesion closes the mouth of Beroë, a carnivorous marine
jelly. Biol Bull Mar Biol Lab Woods Hole 181:463–473 with permission
from the publisher.
Fig. 2. Beroë sp. Gloria (lower) eating a Mnemiopsis (upper). A.
The wide lips of Beroë touch the lobes of Mnemiopsis. B. The mouth
opens fully and the stomach cavity expands to begin ingestion. C. The
Mnemiopsis is half swallowed and is visible inside Beroë’s stomach. D.
The entire Mnemiopsis is engulfed and the bloated Beroë closes its
mouth to swim away. Bar, 5 mm. Reproduced from video tape from
Tamm SL and Tamm S. 199b. Reversible epithelial adhesion closes the
mouth of Beroë, a carnivorous marine jelly. Biol Bull Mar Biol Lab
Woods Hole 181:463–473 with permission.
contributions to adhesion. This symmetric interaction
is evident by forcibly pulling apart excised lips from two
mouths, cutting each lip in half, and then testing for
contra- vs. ipsilateral re-adhesion. After 10–15 minutes
of contact, the two halves of one lip stick to each other
as firmly as do lip halves from opposite sides of the
mouth, showing that any part of the epithelium is
similarly adhesive.
The epithelial cells within each adhesive strip are
linked laterally by adherens-like junctions encircling
their apical ends. The junctional membranes are lined
by dense cytoplasmic coats of microfilaments (Tamm
and Tamm, 1993a; see also Hernandez-Nicaise et al,
1989).
cells and/or cell extensions (DeRosier and Tilney, 1984;
Elson, 1988; Janmey, 1991). The actin filaments underlying the plasma membranes of the adhesive cells
probably serve to mechanically stabilize and strengthen
the highly-folded interdigitating surfaces of these cells.
Such reinforced interlocking of the cell cortices would
provide a stable closure mechanism that fastens the
paired epithelial strips together like a jigsaw puzzle,
independent of tonic muscular activity. Indeed, Mg2⫹relaxed Beroë swim forward with their mouth tightly
closed (Tamm and Tamm, 1991b).
The adhesive strips are probably not held together by
their interlocking geometry alone, but by specific molecular interactions as well. We recently tested the
requirement for extracellular Ca2⫹ in epithelial adhesion to investigate Ca2⫹-dependent cell-cell adhesion
molecules such as cadherins, selectins, and some integrins. In preliminary experiments we found that Ca2⫹-
MECHANISM OF ADHESION
Actin filaments provide mechanical stiffness and
support for maintaining the asymmetric shape of many
REVERSIBLE CELL ADHESION IN BEROË
Fig. 3. Zone of adhesion between excised, Mg-relaxed lip pieces of
B. sp. Gloria. The paired lips (left and right) are being pulled apart
with forceps, and are joined symmetrically by the adhesive strips
(arrowheads) on the stretched stomodaeal walls. The lips edges and
macrociliary fields (M) are at the top; the stomodaeum (s) is down.
Scale bar, 165 µm. Reproduced from video tape from Tamm SL and
Tamm S. 199b. Reversible epithelial adhesion closes the mouth of
Beroë, a carnivorous marine jelly. Biol Bull Mar Biol Lab Woods Hole
181:463–473 with permission.
free artificial sea water (Ca2⫹-free ASW) and Ca2⫹-Mg2⫹free ASW caused excised adherent lips of B. sp. Gloria
to open after 10–15 minutes treatment. Ca2⫹-Mg2⫹-free
ASW was more effective in reducing adhesion than
Ca2⫹-free ASW, which contains 100 mM Mg2⫹. Control
lips in ASW remained tightly closed. When returned to
ASW, the Ca2⫹-free ASW-separated lips re-sealed tightly
in 20–30 minutes, but the Ca2⫹-Mg2⫹-ASW-opened lips
only weakly re-sealed after 1 hour. Thus, epithelial cell
adhesion requires extracellular Ca2⫹, which can be
partly substituted for by high Mg2⫹ concentration.
However, we have not yet checked the ultrastructure of
Ca2⫹-free or Ca2⫹-Mg2⫹-free ASW-separated lips to rule
out other, nonspecific effects of low divalent cations on
the tissues.
We also found that treatment of pulled apart lips
with the lectin Concanavalin A prevented re-adhesion
of epithelial adhesive strips, indicating that proteincarbohydrate binding between lectin domains and oligosaccharide chains of membrane glycoproteins may be
involved in lip adhesion.
The above results merely suggest that cadherins
and/or selectins or even integrins could play a role in lip
adhesion. Although homophilic binding by cadherins
most readily fits the observed symmetry of cell adhesion between paired epithelial strips, intrinsically heterophilic interactions by selectins and/or integrins could,
if populations of partners are mixed on both lips
surfaces, render the adhesion functionally homophilic.
The ultrastructure of the adhesive cell appositions in
Beroë, together with the presence of submembrane
actin filaments, more closely resembles cadherin or
295
Fig. 4. Toluidine blue-stained longitudinal thick sections (0.5 µm)
through a closed mouth of Beroë sp. Gloria. A. Lip edges are at left,
lined with macrocilia (M); stomodaeum (S) is to right. The stomodaeal
walls are joined together by paired strips (cut transversely) of thickened epithelia (arrowheads) located inside the lips. B. Higher magnification of thickened, joined stomodaeal epithelial strips. Apposing cell
surfaces make numerous close contacts interrupted by vacuolar
intercellular spaces. Scale bar: A, 100 µm; B, 17 µm. Reproduced from
Tamm SL and Tamm S. 199b. Reversible epithelial adhesion closes the
mouth of Beroë, a carnivorous marine jelly. Biol Bull Mar Biol Lab
Woods Hole 181:463–473 with permission.
integrin-mediated contacts than selectin-based attachments of leucocytes to blood vessels. Selectin-ligand
bridges between blood cells and endothelial cells are
much greater than 10–20 nm (about 100 nm for
P-selectin and PSGL-1 bonds), and a sub-membrane
actin cytoskeleton is not obvious (Springer, 1995). Because integrins are more commonly found in cell-matrix
adhesions (focal contacts) than in cell-cell adhesions
(blood cell-endothelium), cadherins are presently our
favorite candidate for possible adhesion molecules in
Beroë lips.
We plan to do further experiments on the molecular
nature of lip adhesion. In particular, we will use
pan-cadherin antibodies (Geiger, et al 1990) to look for
cadherins in Beroë adhesive strips by immunofluorescence microscopy, and to test whether function-blocking
cadherin antibodies and synthetic peptides prevent lip
adhesion (Mege, et al 1992). In this regard, some
cadherins can certainly function at the high salinity of
sea water: two conventional cadherins have been identified in sea urchin embryos, and anti-cadherin antibodies perturb sea urchin development (Ghersi, et al 1993).
Similar fluorescence and function-blocking/competing
ligand studies will also probe possible involvement of
selectins and integrins in lip adhesion.
296
S.L. TAMM
Fig. 5. TEM of adherent epithelial strips in a closed mouth of B. sp.
Gloria. The zone of adhesion runs diagonally from lower left to upper
right (arrows), and consists of numerous close contacts of the cell
surfaces alternating with vacular intercellular spaces (s). The plasma
membranes at the appositions have a dense cytoplasmic coat. Thin
longitudinal muscles (lm), here cut transversely, run next to the
mesoglea. ⫻9300. Reproduced from Tamm SL and Tamm S. 199b.
Reversible epithelial adhesion closes the mouth of Beroë, a carnivorous
marine jelly. Biol Bull Mar Biol Lab Woods Hole 181:463–473 with
permission.
REVERSIBLE CELL ADHESION IN BEROË
297
MOUTH OPENING
Contact of prey (other ctenophores) with any region
of the lips of a searching Beroë triggers a local muscular
separation of the lips, followed by rapid peeling apart of
the adhesive strips and wide opening of the mouth by
coordinated muscular activity. The entire response
takes 0.2–0.3 second (Tamm and Tamm, 1993a).
Not surprisingly, mouth opening involves active deadhesion of the epithelial strips themselves. TEM of
mouths induced to open by prey (food-opened mouths)
shows a dramatic change in the surfaces of separated
adhesive strips (Tamm and Tamm, 1993a). No traces of
the specialized appositions remain, nor is there any
evidence of disruption or tearing apart of the cell
surfaces. Instead, the plasma membranes of the adhesive cells appear uniformly smooth and intact without
any sign of the filamentous cytoplasmic coats (Fig. 9).
Rhodamine phalloidin staining is also missing in the
separated adhesive strips of food-opened mouths (Fig.
7C) (Tamm and Tamm, 1993a).
Thus, the interdigitated topography and submembranous actin coat of the cell contacts are rapidly lost—
within 0.2–0.3 second—when the mouth opens to engulf prey. However, the actin-coated junctions encircling
the apical sides of the epithelial cells remain intact
after mouth opening, showing the selective nature of
the control of cell adhesion and actin cytoskeleton in
these cells (Fig. 9) (Tamm and Tamm, 1993a).
In contrast to food-opened mouths, the adhesive cell
appositions and submembrane actin coat do not disappear when the mouth is forcibly opened in the absence
of prey. Instead, the still-adherent contacts are ripped
off the cells, leaving remnants of intact appositions on
either lip (Figs. 7B, 8) (Tamm and Tamm, 1993a). As
noted above, pulled apart mouths or lips will gradually
close and re-adhere within 10–15 minutes, showing the
well-developed wound-healing and regenerative powers of ctenophores (cf. Coonfield, 1936).
Therefore, disassembly of membrane appositions and
actin coats in food-opened adhesive strips cannot be due
simply to mechanical forces arising from mouth opening, but must be signaled by the animal itself, before
muscular separation of the lips.
DE-ADHESION AND MOUTH OPENING
The rapid disappearance of the cortical actin cytoskeleton of adhesive cells upon food-induced mouth opening
should weaken or collapse the highly-folded surface
architecture of these cells. Withdrawal of mechanical
support for the jigsaw-like interdigitations of adherent
strips should diminish their binding and facilitate their
separation when the lips are peeled open by muscular
activity. Disassembly of the submembrane actin net-
Fig. 6. Membrane appositions of adherent epithelial cells in closed
mouths of B. sp. Gloria. The apposed plasma membranes run parallel
to each other and are separated by a distance of about 15 nm, even
when folded and interdigitated (A). The cytoplasmic side of the
membranes is coated with dense material containing microfilaments,
which are particularly evident in oblique or tangential views (C, D).
The intercellular space is often filled with flocculent material that
sometimes appears periodically arranged (A,C). A, ⫻108,400; B,
⫻93,400; C, ⫻86,700; D, ⫻69,000. Reproduced from Tamm SL and
Tamm S. 199b. Reversible epithelial adhesion closes the mouth of
Beroë, a carnivorous marine jelly. Biol Bull Mar Biol Lab Woods Hole
181:463–473 with permission.
298
S.L. TAMM
work should also eliminate the cell binding activity of
possible cadherins and integrins. Cadherin and integrinmediated cell adhesion requires linkage of cytoplasmic
domains of these proteins, via attachment proteins, to
actin filaments, and thus may be regulated by the state
of the actin cytoskeleton (Nagafuchi and Takeichi,
1989; Takeichi, 1990; Alberts, et al 1994).
Fig. 7. Rhodamine-phalloidin fluorescence of epithelial adhesive
strips (as) on the inner surface of lips of B. sp. Gloria. The adhesive
strips run diagonally from upper left to lower right in each image. A.
From a closed mouth: the surface of the adhesive zone shows uniform,
diffuse actin staining. Note fluorescence of belt-like circular muscles
and narrow longitudinal muscles in the mesoglea. B. Pulled apart lip:
large dark holes in the fluorescent adhesive strip correspond to
ripped-off actin-coated appositions on the complementary lip (see Fig.
8). C. Food-opened lip: the uniform actin fluorescence has completely
disappeared from the surface of the adhesive zone. Only the pattern of
circular and longitudinal muscles remains in the background. Bar, 25
µm. Reproduced from Tamm SL and Tamm S. 199b. Reversible
epithelial adhesion closes the mouth of Beroë, a carnivorous marine
jelly. Biol Bull Mar Biol Lab Woods Hole 181:463–473 with permission.
REGULATION OF TISSUE ADHESION
How does prey trigger rapid de-adhesion of the
epithelial strips and muscular opening of the mouth?
We recently discovered a giant fiber nerve net that may
mediate this response (Tamm and Tamm, 1995). TEM
reveals a plexus of 6–8 µm diameter neurons (giant by
ctenophore standards!) that underlies the epithelium of
the adhesive strips (Figs. 10, 11), but not that of the
general stomodaeum, and is apparently a regional
specialization of the much finer stomodaeal nerve net.
Individual giant axons can make synaptic contacts with
both longitudinal muscles which run next to the mesoglea, and epithelial adhesive or gland cells (Fig. 10).
This is the first example to our knowledge of a neuron
contacting more than one type of effector cell. The
synapses, identified by their ultrastructure, have the
characteristic ‘‘chemical’’ transmission morphology of
other presumed nervous elements in ctenophores (Fig.
11) (Hernandez-Nicaise, 1973).
Feeding is initiated by contact of prey with mechanoand chemoreceptors on the outer edge of the lips (Tamm
and Tamm, 1991b; 1993a). The presumed receptor cells
bear bristle-like actin-filled projections, as well as cilia
with unusual onion-like basal structures (HernandezNicaise, 1974; Horridge, 1965b; Tamm and Tamm,
1991a). These cells may therefore function as both
mechanoreceptors and chemoreceptors, i.e., as double
sensory receptors.
The presumed receptor cells make synaptic contacts
with small neurites of the ectodermal nerve net (Hernandez-Nicaise, 1974; Tamm and Tamm, 1991a). If
these neurites are connected to the giant nerve net in
the stomodaeal adhesive strips, then sensory receptors
on the lips could initiate signals that are rapidly
conducted by the giant fiber system to both epithelial
cells and longitudinal muscles in the adhesive strips. A
multi-effector giant fiber nerve net may thus serve as a
final common pathway to rapidly signal de-adhesion of
the epithelial strips as well as contractions of longitudinal muscles underlying the adhesive strips, thereby
enabling Beroë to open its mouth quickly to engulf prey.
How might nervous signals trigger disappearance of
the actin-based, interlocking contacts of adhesive cells?
Since the giant neurons synapse onto the bases of the
epithelial cells, a signal (or signals) must travel 20–25
µm to the apical cell surface and cause disassembly of
the appositions within 0.2–0.3 seconds.
The remarkable speed of this process requires an
electrical response (active or electrotonic membrane
depolarization) of the adhesive cells. The subsequent
intracellular messengers and pathways that mediate
the rapid changes in cell-cell contacts and adhesion are
unknown. Nor do we know whether disappearance of
the cortical actin cytoskeleton is due to complete depolymerization of actin filaments, or rapid turnover and
remodeling into a different pattern elsewhere in the
cell.
REVERSIBLE CELL ADHESION IN BEROË
299
Fig. 8. TEM of a pulled apart adhesive strip, showing intact
appositions (paired arrowheads), vacuolar spaces and cytoplasmic
remnants (cr) ripped off the missing strip. ⫻15,100. Inset: Higher
magnification of a ripped-off apposition on a pulled-apart strip,
showing the dense cytoplasmic coats of the apposed plasma mem-
branes (paired arrowheads). ⫻43,300. Reproduced from Tamm SL and
Tamm S. 199b. Reversible epithelial adhesion closes the mouth of
Beroë, a carnivorous marine jelly. Biol Bull Mar Biol Lab Woods Hole
181:463–473 with permission.
Actin filament-severing proteins of the gelsolin and
ADF (actin-depolymerizing factor)/cofilin families are
known to promote rapid actin filament turnover and
reorganization in many cellular responses to a wide
variety of stimuli and cell signaling molecules (Moon
and Drubin, 1995; Puius, et al 1998; Welch, et al 1997).
These actin-binding proteins serve as stimulus-responsive modulators of actin dynamics, and are therefore
prime candidates for mediating the rapid loss of actinsupported appositions of Beroë adhesive cells in response to prey.
Gelsolin’s actin-severing activity is activated by Ca2⫹
(Yin and Stossel, 1979). Ca2⫹ influx through voltagedependent Ca2⫹ channels, triggered by membrane depolarization, can induce gelsolin-mediated actin depolymerization in neurons (Bernstein and Bamburg, 1985;
Furukawa, et al 1997; Neely and Gesemann, 1994).
ADF/cofilin is functionally regulated by pH, polyphosphoinositides, and phosphorylation (Aizawa, et al 1997;
Moon and Drubin, 1995). In the latter case, stimulusevoked Ca2⫹ influx, via calmodulin-dependent protein
phosphatase, can induce rapid dephosphorylation of
ADF/cofilin, thereby activating it and causing rapid
reorganization of the actin cytoskeleton (Meberg, et al
1998; Moon and Drubin, 1995).
Activation of ADF/cofilin is not only temporally regulated by signaling pathways, but spatially regulated as
well. Dephosphorylated active ADF/cofilin somehow
translocates to appropriate regions of the cell where it
promotes actin filament turnover and remodeling (Abe,
et al 1996; Nebl, et al 1996; Samstag, et al 1994; Suzuki,
et al 1995). In cAMP-induced chemotaxis of Dictyostelium, GFP-cofilin redistributes into new pseudopods
in 30–60 seconds (Aizawa, et al 1997). In stimulusactivated neutrophil-like HL-60 cells, cofilin is translocated
from the cytosol to the plasma membrane of the leading
edge in less than 30 seconds (Suzuki, et al 1995).
In Beroë, giant neuron synaptic activity at the bases
of adhesive cells might trigger depolarization and opening of voltage-gated Ca2⫹ channels at the apical surfaces, perhaps in the vacuolar intercellular spaces
surrounding the appositions. Ca2⫹ influx from the
vacuolar fluid (sea water?) could activate gelsolin and/or
ADF/cofilin, with or without subsequent translocation,
leading to rapid loss of the actin filament coat in the
appositions.
A major difference, however, between previously described changes in the actin cytoskeleton and that of
Beroë adhesive contacts is speed of the response. The
disassembly of the submembranous actin coat and cell
300
S.L. TAMM
Fig. 9. TEM through the apical end of a food-opened adhesive
strip. The appositions have disappeared, and the plasma membrane is
smooth and unfolded without a dense cytoplasmic coat. Encircling belt
junctions between epithelial cells remain, however (arrowheads).
⫻23,500. Reproduced from Tamm SL and Tamm S. 199b. Reversible
epithelial adhesion closes the mouth of Beroë, a carnivorous marine
jelly. Biol Bull Mar Biol Lab Woods Hole 181:463–473 with permission.
appositions in food-opened epithelial adhesive strips
must occur before, or during muscular separation of the
lips, i.e., in less than 0.2–0.3 seconds. This is approximately 100-fold faster than the most ‘‘rapid’’ or ‘‘dynamic’’ reorganizations of actin cytoskeletons reported
so far. The question is, does Beroë use novel processes to
regulate its actin cytoskeleton and cell-cell adhesion so
quickly? We hope to find the answer.
no physiological evidence yet that it signals deadhesion.
As noted above, the interlocking close appositions of
the adhesive cells are not continous, but are interrupted by irregular intercellular gaps whose membranes are not lined by dense actin coats. These vacuolar spaces probably do not contribute to adhesion of
the epithelial strips. Why are they present? The intercellular spaces may serve to increase the surface area of
the paired adhesive strips without unduly increasing
their adhesive strength. Wider strips would be more
likely to overlap and reestablish contact after the
mouth of a bloated Beroë closes over prey. In fact,
sections through closed mouths often show a slight
offset or mismatch between opposing adherent strips
(Fig. 4; Tamm and Tamm, 1991b). If the adherent
surfaces were continuous without intervening spaces,
the strips themselves would be much narrower, and
more likely to miss one another upon closure of the
stretched stomach walls after ingestion.
REVERSIBILITY AND RE-ADHESION
After engulfing prey, Beroë’s mouth closes and the
lips re-seal. We have not yet examined the process of
re-adhesion of food-opened epithelial strips, so we do
not know how the submembranous actin cytoskeleton
and interdigitating surface appositions reform. Formation of the elaborately sculptured, interlocking surfaces
of apposed adhesive cells may be driven by localized
polymerization of membrane-associated actin. It is well
known that polymerization and/or remodeling of actin
networks can cause changes in cell shape and architecture (Tilney and Inoue, 1982; Welch, et al 1997; Wyman,
et al 1990). It will be informative to test agents that
inhibit actin polymerization (cytochalasin D, latrunculin) on reformation of actin-based appositions after
feeding.
Whether the giant neuron system is involved in
signaling re-adhesion remains unknown, but we have
SIGNIFICANCE
We may ask first, not what Beroë’s epithelial strips do
for understanding the dynamics of cell adhesion and
actin cytoskeleton, but what do they do for Beroë?
At the moderate Reynolds number of a cruising
Beroë, the streamlined body shape should reduce drag
REVERSIBLE CELL ADHESION IN BEROË
301
Fig. 10. Giant neuron lattice (gn) underlying the epithelial adhesive strip. The neuronal branches are continuous and filled with clear
vesicles and parallel arrays of microtubules which diverge at intersec-
tions to follow the branches. Neuronal branches running perpendicular to longitudinal muscles (lm) interrupt the fibers. Note synapses
onto adhesive cells and muscles (arrowheads). Scale bar, 1 µm.
and save energy. In thin-walled beroids with stomodaeal adhesive strips, mouth closure does not require
muscular or neural activity. Epithelial adhesion thus
seems a useful and efficient method for closing the
mouth and streamlining the body of an active gelatinous predator that spends most of its time swimming
mouth forward in search of prey.
In contrast, beroids with a thicker body wall, cucumber-shaped body, and smaller mouth (B. cucumis, B.
gracilis) do not have stomodaeal adhesive strips. Neither the lips nor the stomach walls are fastened together in any manner (Tamm and Tamm, 1991b).
Evidently, the thicker, firmer body and smaller oral
opening provide sufficient resistance to maintain normal body shape during forward swimming, without the
need for epithelial adhesion.
What Beroë’s mouth can do for us as cell biologists is
more relevant here. Reversible tissue adhesion in Beroë
shares many structural and functional properties with
transient adhesions made between migrating cells in
developing embryos of higher animals, wound closure
after injury in adult tissues, inflammatory responses,
and tumor growth. In all these cases, cell contacts
generally do not involve formation of structurally differentiated intercellular junctions, but instead employ
nonjunctional appositions, in which adjoining plasma
membranes come close together and run parallel, separated by a 10–20 nm space. Submembrane actin filament networks are a common feature in such appositions (Alberts, et al 1994; Heaysman and Pegrum
1973a, 1973b). ‘‘This type of nonjunctional contact may
be optimal for cell locomotion—close enough to give
traction but not tight enough to immobilize the cell’’
(Alberts, et al 1994, p. 971). Because the apposed cell
membranes of Beroë adhesive strips and moving cells in
other systems are not structurally bound to one another, ‘‘bonds between the cell surfaces in such appositions would be more readily made and broken and
remade again than in junctions’’ (Trinkaus, 1984, p.
171). These nonjunctional cell-cell contacts are thus ‘‘a
prime candidate for the kind of adhesion that moving
cells require’’ (Trinkaus, 1984, p. 171). Similarly, such
appositions would seem well-designed for the reversible
type of tissue adhesion required to close and open the
mouth of Beroë.
Unlike the other systems of transient cell-cell adhesions cited above, however, the epithelial strips of Beroë
involve thousands of cells all doing the same thing—
adhering or de-adhering—at the same time in response
to readily controllable external stimuli. The same re-
302
S.L. TAMM
Fig. 11. Multiple synapses (arrowheads) of a giant neuron (gn)
onto neighboring adhesive cells (ac) wedged between longitudinal
muscles (lm). Note the characteristic ‘‘presynaptic triad’’ composed of a
single layer of synaptic vesicles at the cleft, a flattened sac of smooth
ER, and one or more closely apposed mitochondria; arrowheads
indicate synaptic polarity (see Hernandez-Nicaise, 1973). Scale bar, 1
µm. Reproduced from Tamm SL and Tamm S. 199b. Reversible
epithelial adhesion closes the mouth of Beroë, a carnivorous marine
jelly. Biol Bull Mar Biol Lab Woods Hole 181:463–473 with permission.
gions of the same cells continually and reversibly make
and break adhesive contacts. De-adhering epithelial
strips show the fastest change in actin-based cell-cell
adhesion yet reported. The mouth of Beroë therefore
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ACKNOWLEDGEMENTS
This review is dedicated to G.A. Horridge, a Dionysian and pioneer of structure and function in nervous
systems of invertebrates.
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