вход по аккаунту



код для вставкиСкачать
THE ANATOMICAL RECORD 249:117–127 (1997)
Golgi–Canalicular Reticulum System in Ion Transporting Fibrocytes
and Outer Sulcus Epithelium of Gerbil Cochlea
Department of Pathology and Laboratory Medicine, Medical University of South Carolina,
Charleston, South Carolina
Background: Five types of highly specialized fibrocytes
have been identified in the spiral ligament of the gerbil cochlea. Type I, II,
and IV fibrocytes function in cycling back to the stria vascularis K1
effluxed from outer hair cells and nerves during auditory transduction.
Thus, evidence exists for a transcellular path of K1 movement from outer
sulcus cells through fibrocytes to the strial interstitial space, but a
mechanism for facilitating such ion flow within the cells has not been
Methods: The spiral ligament of glutaraldehyde–osmium tetroxide-fixed
and Epon-embedded gerbil cochlea was examined by transmission electron microscopy.
Results: Ultrastructural examination disclosed an extensive membrane
limited reticulum in the cytoplasm of type I, II, IV, and V fibrocytes of the
lateral wall and in outer sulcus cells and their root processes. This system
resembled the tubulocisternal endoplasmic reticulum present in some
ion-transporting epithelia but appeared more to constitute a network of
canaliculi and is referred to as the canalicular reticulum (CR). Many
typical small Golgi complexes invariably accompanied the CR in the
fibrocytes and sulcus cells, as we have found to be true of other epithelia
known to contain CR and function in ion transport. Numerous mitochondria populated cytosol-containing CR.
Conclusions: The data support the concept of transcellular K1 flux in
type I, II, IV, and V fibrocytes and outer sulcus cells in the cochlea and lend
credence to the view of CR as functioning in the movement of ions through
cells. The constant and precise association of Golgi complexes with CR in
the different cell types implies a functional relationship possibly concerned with biosynthesis of CR by Golgi elements, and the abundance of
mitochondria near CR indicates an energy requirement for function of the
reticulum or its biosynthesis. Anat. Rec. 249:117–127, 1997.
r 1997 Wiley-Liss, Inc.
Key words: inner ear; spiral ligament; ultrastructure; electrolytes; ion
Maintenance of the K1 gradient between endolymph
and perilymph is essential for normal hearing and
depends primarily on activity of the stria vascularis (for
review, see Marcus, 1986; Wangemann et al., 1995).
Abundant Na,K-ATPase in the stria (Inuma, 1967;
Kuijpers and Bonting, 1969) and more precisely the
basolateral plasmalemma of strial marginal cells (Kerr
et al., 1982; Schulte and Adams, 1989; Nakazawa et al.,
1995) provides a pumping mechanism for preserving
the 150 mM K1 level unique to endolymph among
extracellular body fluids. Fibrocytes in the spiral ligament of the cochlea appear to function in supplying K1
to the strial pump by cycling back to the stria (Schulte
and Steel, 1994; Spicer and Schulte, 1994, 1996) ions
that efflux from scala media during auditory transducr 1997 WILEY-LISS, INC.
tion (Konishi et al., 1978; Wada et al., 1979; Marcus,
1986; Salt and Konishi, 1986; Sterkers et al., 1988).
The lateral wall of the cochlea encloses five types of
fibrocytes that have been differentiated on the basis of
location, ultrastructural features, and content of enzymes that mediate or energize ion transport, including
Na,K-ATPase, carbonic anhydrase, and creatine kinase
Contract grant sponsor: National Institute on Deafness and Other
Communication Disorders, National Institutes of Health; Contract
grant number: DC00713; contract grant number: DC00422.
*Correspondence to: Dr. Samuel S. Spicer, Department of Pathology
and Laboratory Medicine, Medical University of South Carolina, 171
Ashley Avenue, Charleston, SC 29425.
Received 25 November 1996; accepted 14 March 1997.
(Spicer and Schulte, 1991, 1996) (Fig. 1). Evidence
indicates that plasmalemmal Na,K-ATPase of type II
fibrocytes functions to lower K1 in fluid bathing outer
sulcus cells and thereby promote K1 efflux from these
cells, while also creating an elevated intracellular K1
level from which the ion diffuses down gradient to type I
fibrocytes enroute to strial basal and marginal cells.
Extensive plasmalemmal foldings that increase the
ATPase-rich surfaces of type II fibrocytes bordering
outer sulcus cells and the contact of branching narrow
expansions from the inferior pole of type II fibrocytes
with type Ib fibrocytes fit with the view of K1 flow from
sulcus cells through polarized type II fibrocytes and
downgradient to type Ia fibrocytes. Broad and narrow
contacts (Spicer and Schulte, 1996) and gap junctions
(Iurato et al., 1976; Nadol, 1978; Santos-Sacchi and
Dallos, 1983; Kikuchi et al., 1995) between fibrocytes
and between these cells and strial basal cells further
testify to the possibility of diffusion of K1 through the
fibrocytes to the stria vascularis.
The available data thus point to K1 return to the
stria vascularis in the lateral wall via a transcellular
rather than an extracellular route. How structural and
biochemical characteristics favor an intracellular rather
than extracellular path has not been explained. Further inquiry into the fine structure of lateral wall cells
reported in the present study delineates a previously
undetected system of membrane-limited cisternal elements that apparently constitute a reticulum and
possibly relate to ion circulation in these cells.
The Mongolian gerbils (Meriones unguiculatis) used
in the present study were housed in a low-noise room
from birth to death at 3–6 months of age. Similarly aged
animals from the gerbil colony maintained in this
facility have consistently shown normal hearing as
judged by evoked potentials of brainstem and auditory
nerve (Schmiedt, 1989; Mills et al., 1990; Boettcher et
al., 1993). Procedures for the care and use of animals
were approved by the Animal Use Committee of the
Medical University of South Carolina under NIH grant
DC 00713.
The gerbils under urethane anesthesia (1.5 gm/kg,
i.p.) were perfused with minimal pressure via a cardiac
catheter employing 10 ml of near-body-temperature
0.9% saline solution that contained 0.1% NaNO2. After
exsanguination, the bodies were perfused with 50 ml of
room-temperature fixative fluid consisting of freshly
depolymerized 4.0% paraformaldehyde and 2.0% glutaraldehyde in 0.1 M phosphate buffer, pH 7.4. The bullae
were then opened, the stapes was removed, the round
window was perforated, and 1.0 ml of fixative was
injected gently into the oval window until it escaped
through the round window. The cochleas were dissected
free and immersed in fixative overnight in the refrigerator. The scalae were subsequently flushed gently with
phosphate buffer, and the inner ears were trimmed of
excess bone and decalcified by perfusion with and then
immersion in 0.12 M EDTA, pH 7.0, containing 0.2%
glutaraldehyde. The EDTA solution was changed every
48 hr until decalcification was complete (about 2 weeks).
The specimens were bisected along the plane of the
modiolus with a razor blade. To reduce compressive
distortion of the organ of Corti during bisection, the
Fig. 1. Distribution of type Ia, Ib, II, III, IV, and V fibrocytes differs in
gerbil cochlea at the 500-Hz place, providing three routes for ion
transport toward the stria vascularis. Na,K-ATPase-rich type II, IV,
and V fibrocytes serve in the context of a pumping station to draw
electrolytes from the organ of Corti, Hensen, Claudius, and outer
sulcus cells (large arrows), from scala tympani (small arrows), and
from scala vestibuli (arrowheads) and to move the ions into type Ib
fibrocytes enroute to the stria (Spicer and Schulte, 1996). Inset shows
suprastrial type V fibrocytes overlying type Ib fibrocytes. CC, Claudius
cells; OSC, outer sulcus cells and roots; SP, spiral prominence; StV,
stria vascularis; SM, scala media; ST, scala tympani; SV, scala
vestibuli. Toluidine blue-stained epoxy thick section. 3470. Inset,
scalae were perfused with warm (45°C) 10% gelatin
(300 bloom) and then chilled on an ice bath until the
gelatin congealed. Following bisection, the gelatin was
removed from the half cochleas by agitation in phosphate buffer warmed to approximately 45°C. The tissue
was immersed in 0.8% orcein in acetic acid/alcohol for 3
min (Clark, 1960), rinsed, and placed in 1% osmium
tetroxide in buffer for 30 min, washed in distilled water,
then dehydrated and embedded in Epon resin. Prior to
complete polymerization of the resin, the cochleas were
sliced into individual half-turns and reembedded in
resin in a slide mold to facilitate subsequent viewing of
the tissue as a surface preparation. The cochleas were
mapped, and radial slices were cut with a razor blade
from cochlear regions encoding 0.5–20 kHz (Tarnowski
et al., 1991). These slices were reembedded in Epon.
Thick sections and adjacent thin sections were taken
at several levels, 25 µm apart from each epoxy block,
and the thick sections were stained with toluidine blue.
Ultrathin sections were selected for electron microscopic examination and stained with uranyl acetate
and lead citrate when the adjacent thick section displayed a full-length view of well-preserved spiral ligament and stria vascularis. Sections were examined
ultrastructurally from three cochleas at the 2-, 10-, and
20-kHz regions.
Type Ia fibrocytes contacted strial basal cells extensively (Fig. 1) at gap junctionlike connections (Fig. 2).
The Ia fibrocytes made similar but narrower contact
with one another throughout the underlying spiral
ligament (Fig. 3). The fibrocytes bordering basal cells
enclosed membrane-limited profiles that appeared to
constitute a network of canalicular structures (Fig. 2).
In some Ia fibrocytes more removed from the stria, this
canalicular reticulum (CR) occupied an axial core in the
cell (Fig. 3). Numerous mitochondria infiltrated CRrich areas (Fig. 2, inset at right), and in longitudinal
fibrocyte profiles, the mitochondria showed moderate to
extreme elongation in the direction of the long axis of
the fusiform cell (Fig. 3).
Some Ia cell profiles exhibited Golgi complexes possessing a distinctive fine structure. These complexes
commonly consisted of one or two neighboring stacks of
about five short cisternae (Fig. 2, inset at left). Occasional wider complexes formed a shallow arch. One face
of the Golgi complex often consisted of an uninterrupted cisterna and the other of a segmented cisterna
or adjacent aligned vesicles. The Golgi zones occupied
cytosolic areas near profiles of CR.
Type Ib fibrocytes located inferior to Ia and superior
and deep to IIb fibrocytes (Fig. 1) differed from the Ia
cells in their lesser asymmetry and more abundant
perinuclear cytosol and mitochondria (Figs. 4 & 5) and
in their contact by slender processes from type II
fibrocytes (Fig. 6). A reticulum of canalicular profiles
filled much of the cytosol of Ib fibrocytes (Fig. 4) most
densely as a rule in a perinuclear location (Fig. 5).
Distribution of the CR corresponded closely with that of
numerous mitochondria (Figs. 4 & 5). Golgi zones of Ib
resembled those of Ia fibrocytes in structure and in
their abundance in cell locations endowed with CR
(Fig. 4).
Type IIb fibrocytes occurred in the spiral prominence
area. These cells showed structural polarity by their
plasmalemmal outfoldings from the superior and lateral surfaces of the elongated cell body, where it closely
neighbored outer sulcus cells (Fig. 7). In contrast to
their upper segments, type IIb fibrocytes extended from
their inferior pole slender processes that contacted Ib
fibrocytes (Fig. 6). Prominent profiles of CR spread
throughout the cytosol (Figs. 7, 8, & 10), extending in
lesser abundance into small cell branches but not into
the plentiful villuslike protrusions of plasmalemma
(Figs. 6–10). Some profiles of type II fibrocytes enclosing widespread CR (Fig. 7) differed from others in
displaying less prevalent canalicular and more abundant vesicular structures.
Type IV and V fibrocytes are thought to function like
type II fibrocytes but to serve in facilitating electrolyte
flow to type I fibrocytes from scala tympani and scala
vestibuli, respectively, rather than from organ of Corti
(Spicer and Schulte, 1996; Fig. 1). The type IV and V
fibrocytes also enclosed profiles of CR.
Numerous mitochondria infiltrated in greater density the CR-rich region bordering one pole of the
nucleus in longitudinally sectioned type II fibrocytes
(Figs. 7 & 8). Mitochondria located in paranuclear
cytosol containing a dense concentration of CR and
prominent Golgi elements appeared smaller and less
asymmetric than mitochondria in the distal slender
processes of IIb fibrocytes (Figs. 7 & 10).
An exceptional abundance of distinctive Golgi zones
that otherwise resembled those in type I cells in their
small size, organization, and distribution with the CR
characterized type II fibrocytes. A cell displaying greater
prevalence of vesicular than cisternal membranous
elements showed especially numerous Golgi zones (Fig.
7). The Golgi complexes appeared confined to a region of
the cell opposite one end of the nucleus and enriched
with the greatest concentration of mitochondria (Figs. 7
& 8).
Root bundles composed of multiple outer sulcus cell
processes extended into the spiral prominence region
populated by type IIb fibrocytes and dense stromal
strands. The cytologic structure of the root processes
differed widely within a bundle (Galic and Giebel,
1989). Content of CR differed comparably among the
root processes. Some of the processes enclosed abundant profiles of CR, other processes enclosed only
sparse cisternae generally oriented across the process,
and still others did not enclose this organelle (Figs. 11 &
12). Mitochondria infiltrated in greater numbers cytoplasmic regions exhibiting greater volume density of
CR (Figs. 11 & 12). Typical small Golgi complexes
occurred frequently in regions of roots containing prominent CR and mitochondria but not elsewhere (Fig. 11).
A system of membrane-limited tubules and cisternae
referred to as the tubulocisternal endoplasmic reticulum (TCER) has been demonstrated in certain epithelia
by en bloc staining with an uranyl acetate/PbNO2/
CuSO4/OsO4 sequence (Møllgård and Rostgaard, 1978).
Although the TCER in these cells in general resembled
the system observed in the present study in routinely
processed tissue, the membranous profiles in the cochlear fibrocytes and sulcus cells appeared to consist
mainly of branching and interconnected canals. As
indicative of the system’s structure and perceived function, the term ‘‘canalicular reticulum’’ seems preferable
Fig. 2. A type Ia fibrocyte apposed at gap junctions (arrowhead) to
strial basal cells (BC) encloses profiles of canalicular reticulum (CR;
arrows) and fairly numerous interspersed mitochondria. Inset at
lower left shows a typical Golgi zone from a Ia fibrocyte and that at
lower right shows more detail of branching elements of CR and many
associated mitochondria. 38,000. Left inset, 318,750. Right inset,
Fig. 3. A longitudinally sectioned type Ia fibrocyte in the midregion
of spiral ligament joins other Ia fibrocytes via gap junctions (arrowheads) and contains a central core of CR, with neighboring mitochondria elongated parallel to the long axis of the cell. 310,000.
at least for the cochlear cells and is employed in the
present study.
TCER has been interpreted as promoting transcellular flow of fluid and ions. The organelle has been
implicated in Na1 transport in frog skin (Voûte et al.,
1975) and fluid and ion movement across ileal epithelium (Møllgård and Rostgaard, 1981). It has been
visualized in hepatocytes (Møller et al., 1983) and in
ion-transporting epithelium of the gallbladder, choroid
plexus, proximal renal tubule (Møllgård and Rost-
Fig. 4. A type Ib fibrocyte discloses CR densely and evenly distributed throughout the cell body and approaching close to the plasmalemma. Golgi complexes (arrows) consist of compact stacks of a few
short cisternae. Inset shows a fibrocyte’s Golgi complex at higher
magnification. 38,500. Inset, 337,500.
Fig. 5. In a transversely sectioned type Ib fibrocyte, CR and interspersed mitochondria encircle the central nucleus. 35,500.
Fig. 6. Slender processes of type IIb fibrocytes identified in part by
their large dark mitochondria extend between and make gap junctionlike contact (arrowheads) with Ib fibrocytes. Elements of CR populate
the type II fibrocytes but not the plasmalemmal foldings from these
cells. The inset shows processes from a IIb fibrocyte abutting on a Ib
fibrocyte below. 38,000. Inset, 313,750.
Fig. 7. A longitudinally sectioned IIb fibrocyte, closely bordering the
dense stromal fibers that envelope a root bundle (RB), possesses
extensive membranous elements. These take the form of cytoplasmic
vesicles or cross-sectioned tubules more than canaliculi except at the
poles of the cell. Numerous short, compact Golgi stacks (arrows)
intermingle with densely populated mitochondria opposite one pole of
the nucleus. Evaginations of the plasmalemma amplify the cell
surface. Insets show details of Golgi complexes of type II fibrocytes.
310,500. Upper inset, 334,000. Lower inset, 330,000.
gaard, 1978, 1981; Rostgaard and Møllgård, 1980;
Bergeron and Thiéry, 1981), and human eccrine sweat
gland (Baron et al., 1984). In the cochlea, strial marginal cells (Forge, 1982) and Reissner’s epithelium
(Qvortrup and Rostgaard, 1990) contain TCER. The CR
shown in cochlear fibrocytes and sulcus cells resembles
TCER and presumably functions similarly in mediating
ion and fluid movement.
TCER has been described only in polarized epithlelial
cells, where it presumably directs ion translocation
between luminal and abluminal surfaces. Because fibrocytes lack the polarity that is established in epithelia by
tight junctions, they would seem not to require or be
adapted to utilize TCER. However, the abundant canalicular network demonstrated in the present study in
the specialized fibrocytes of the cochlear spiral ligament can be assumed to perform like that in epithelia
and to provide thereby an indication of polarized transport activity in these cells. Support for this perception
stems from the evidence (Spicer and Schulte, 1996) in
type IIb fibrocytes of a structural polarity thought to
underlie a capacity for directing ion flow. The position
and fine structure of IIb fibrocytes point to such a
possibility. Thus, the upper end of these asymmetric
cells, where they border outer sulcus cell roots, exhibited marked surface expansion in the form of plasmalemmal evaginations in contrast to the lower pole of the
cell, which contacted type I fibrocytes at the end of cell
process arborizations (Fig. 6). Type II fibrocytes apparently resorb at their superior pole K1 effluxing from
root bundles and release the ion through gap junctions
with Ib fibrocytes at the opposite end of the cell.
Such a prominent system of CR in spiral ligament
cells must contribute importantly to their bioactivity.
Whether the rate of extracellular K1 diffusion to the
stria through a tissue densely populated with cells and
interstitial fibers would suffice for the strial Na,KATPase pump to maintain the 150 mM K1 of endolymph is open to question, as is the supposition that the
rate of diffusion through cytosol would contribute a
significant advantage over extracellular flow. A network such as the CR offers a means of channeling
Fig. 8. A longitudinally sectioned IIb fibrocyte exhibits an elaborate
array of branching, interconnected canaliculi, and numerous vesicles.
These elements of CR spread throughout the cytosol. Frequent,
relatively short Golgi stacks (arrows) intermingle with CR on one side
of the nucleus in an area containing CR and the densest collection of
mitochondria. Plasmalemmal outfoldings protrude from the cells.
Inset shows an abundance of Golgi complexes (arrows) in a CR-rich
area containing many mitochondria. 318,000. Inset, 316,000.
Fig. 9. CR occurs in processes of type IIb fibrocytes but not the plasmalemmal outfoldings (arrowheads)
from these cells. 39,500.
Fig. 10. Numerous profiles of CR border the poles of the nucleus in a IIb fibrocyte. Mitochondrial profiles
near this CR (arrows) appear smaller than those in more narrow and distal cell processes (arrowheads).
Fig. 11. One root process (arrow) in a root bundle differs from others
in containing numerous mitochondria and profiles of CR with associated Golgi zones (arrowheads). Prevalence of elements of CR among
the root processes parallels that of mitochondria and of Golgi elements. A IIb fibrocyte adjacent to the root bundle at lower left contains
abundant CR and mitochondria. Inset shows an enlargement of a
Golgi zone from the root bundle. 35,500. Inset, 337,500.
unimpeded K1 diffusion in the cell and influencing the
rate and direction of ion translocation. In addition, the
reticulum provides a mechanism for sequestering electrolytes from cytosol and avoiding a cytotoxic effect of
elevated ion concentration on cell metabolism. In accord with the latter concept is the observation that
Hensen, Claudius, and inner sulcus cells, which lack
CR but conduct electrolyte flow in the cochlea, possess a
lucent cytosol with essentially none of the cytologic
organelles that might suffer from ion toxity (Spicer and
Schulte, 1997).
The finding that some outer sulcus cells and types Ia,
Ib, and II fibrocytes contain CR supports the view that
together these cells constitute a path for the recycling of
K1 back to the stria (Spicer and Schulte, 1996). If this
thesis is correct, the presence of CR in these cell types
provides further evidence for the role of this organelle
in electrolyte transport by cells.
Subsurface cytosol generally separated profiles of
canalicular structures from the plasmalemma. Type II
fibrocytes disclosed little evidence for ion resorption or
secretion through direct fusion of CR elements with
plasmalemma. Therefore, participation of the CR in
moving transcellularly the K1 resorbed by plasmalemmal ATPase in type II fibrocytes should theoretically
require K1 permeability in the membrane delimiting
this system. K1 conductance in the CR membrane could
allow the CR to resorb K1 from cytosol possessing a
high K1 level at the superior pole of the fibrocyte and to
release the ion into cytosol with lower K1 at the inferior
pole. By way of affirming this concept, the plasmalemmal Na,K-ATPase more abundant at the superior end of
the type II fibrocytes functions to maintain there a
relatively high cytosolic K1, whereas gap junctions
lower cytosolic K1 at the inferior pole of these cells by
permitting the ion to escape into Ib fibrocytes.
Whereas identification of TCER required special en
bloc staining, the organelle was visualized in the cochlear fibrocytes and outer sulcus cells in specimens
prepared routinely for electron microscopy. The membra-
Fig. 12. A root from an outer sulcus cell displays profiles of CR,
mitochondria, and microtubules (arrowheads). 330,000.
nous reticulum in the cochlear fibrocytes appeared
labile to tissue processing, however, as it was encountered in abundance in some but only sparsely or not at
all in other specimens.
An increased volume density of mitochondria accompanied the CR in the region of fibrocytes and outer
sulcus cells populated by the reticulum. The codistribution of mitochondria and CR directs attention to transport processes performed by the reticulum, possibly
requiring a source of energy in lateral wall cells.
Extremely asymmetric mitochondria bordered CR profiles closely over a considerable distance in an arrangement consistent with their serving as an energy source
for the membranous system (Fig. 3). However, there is
presently no knowledge that CR contains an ATPase or
a protein kinase, either of which would utilize high
energy phosphate for ion transport, and it is accordingly uncertain as to whether this system demands
energy for its presumed function in facilitating ion flow.
Moreover, the elaborate display of CR in other sites
such as Deiters cells of gerbil cochlea and the human
eccrine sweat gland lack an abundance of closely associated mitochondria (Spicer and Schulte, 1993; Baron et
al., 1984). If mitochondria associated with CR energize
ion movement in type II fibrocytes, the transport mechanism involved in this site must differ from that in
Deiters cells and sweat glands.
Alternatively, mitochondria populating CR-rich areas of cytosol could provide an energy source for biosynthesis of the membranous complex. The abundance of
mitochondria showing a distinctive rounded profile in
paranuclear regions rich in CR and Golgi zones (Figs. 3,
7, & 8) is consistent with such an interpretation. In this
case, information concerning possible differences in
function or rate of turnover is needed for explaining the
more impressive codistribution of mitochondria with
Golgi cisternae in the fibrocytes than in Deiters cells.
Cytoplasmic areas with dense profiles of CR and
mitochondria in all lateral wall cells invariably possessed a few to many Golgi complexes. A similar
association of CR with Golgi elements has been encountered in other sites including human eccrine sweat
glands (Baron et al., 1984) and cochlear Deiters cells
(Spicer and Schulte, 1993). Moreover, a striking development of Golgi cisternae takes place in Deiters cells
and pillar cells of neonatal gerbils 14–15 days after
birth, at the precise time when CR appears in these
cells (Ito et al., 1995). The hyperabundance of both
systems occurred transiently, as they disappeared together from pillar cells during further postnatal development but in Deiters cells persisted into adulthood
with a somewhat diminished volume of Golgi complexes
and associated mitochondria. The codistribution of
Golgi zones and CR in many cell types of the cochlear
lateral wall and elsewhere, the concurrence of Golgi
zones and CR only in a paranuclear area rich in
mitochondria in type II fibrocytes, and the simultaneous timing of the appearance and disappearance of
Golgi zones and CR during postnatal development all
point to a possible role for Golgi cisternae in biosynthesis of the membranous reticulum.
We thank Mrs. Nancy Smythe and Mrs. Leslie Harrelson for their technical and editorial assistance.
Baron, D.A., J.V. Briggman, and S.S. Spicer 1984 Tubulocisternal
endoplasmic reticulum in human eccrine sweat glands. Lab.
Invest., 51:233–243.
Bergeron, M., and G. Thiéry 1981 Three-dimensional characteristics
of the endoplasmic reticulum of rat renal tubule cells, an electron
microscopy study in thick sections. Biol. Cell, 42:43–48.
Boettcher, F.A., J.H. Mills and B.N. Norton 1993 Age-related changes
in evoked potentials of gerbils. I. Response amplitudes. Hearing
Res. 71:137–145.
Clark, G. 1960 Staining Procedures Used by the Biological Stain
Commission. Williams and Wilkins, Baltimore, pp. 63.
Forge, A. 1982 A tubulocisternal endoplasmic reticulum system in the
potassium and transporting marginal cells of the stria vascularis
and effects of the ototoxic diuretic ethacrynic acid. Cell Tissue
Res., 226:375–387.
Galic, M., and W. Giebel 1989 An electron microscopic study of the
function of the root cells in the external spiral sulcus of the
cochlea. Acta Otolaryngol. (Suppl.), 461:3–15.
Iinuma, T. 1967 Evaluation of adenosine triphosphatase activity in the
stria vascularis and spiral ligament of normal guinea pigs.
Laryngoscope, LXXVII:141–158.
Ito, M., S.S. Spicer, and B.A. Schulte 1995 Cytological changes related
to maturation of the organ of Corti and opening of Corti’s tunnel.
Hearing Res., 88:107–123.
Iurato, S., K. Franke, L. Luciano, G. Wermbler, E. Pannese, and E.
Reale 1976 Intercellular junctions in the organ of Corti as
revealed by freeze fracturing. Acta Otolaryngol. (Stockh.), 82:57–
Kerr, T.P, M.D. Ross, and S.A. Ernst 1982 Cellular localization of
Na1,K1-ATPase in the mammalian cochlear duct: Significance for
cochlear fluid balance. Am. J. Otolaryngol., 3:332–338.
Kikuchi, T., R.S. Kimura, D.L. Paul, and J.C. Adams 1995 Gap
junctions in the rat cochlea: Immunohistochemical and ultrastructural analysis. Anat. Embryol., 191:101–118.
Konishi, T., P.E. Hamrick, and P.J. Walsh 1978 Ion transport in guinea
pig cochlea. I. Potassium and sodium transport. Acta Otolaryngol., 86:22–34.
Kuijpers, W., and S.L. Bonting 1969 Studies on (Na1–K1)-activated
ATPase XXIV. Localization and properties of ATPase in the inner
ear of the guinea pig. Biochem. Biophys. Acta, 173:477–485.
Marcus, D.C. 1986 Neurosensory electrophysiology of the cochlea:
Stria vascularis. In: Neurobiology of Hearing: The Cochlea. R.A.
Altschuler, D.W. Hoffman, and R.P. Bobbin, eds. Raven Press,
New York, pp. 123–137.
Mills, J.H., R.A. Schmiedt and L.F. Kulish 1990 Age-related changes in
auditory potentials of Mongolian gerbil. Hearing Res., 46:201–
Møller, O.J., O. Østergaard-Thomsen, and J.A. Larsen 1983 The
existence of tubulocisternal endoplasmic reticulum in rat hepatocytes. Cell Tissue Res., 228:13– 20.
Møllgård, K., and J. Rostgaard 1978 Morphological aspects of some
sodium transporting epithelia suggesting a transcellular pathway
via elements of endoplasmic reticulum. J. Membr. Biol. (Special
Issue), 40:71–89.
Møllgård, K., and J. Rostgaard 1981 The transcellular compartment of
tubulocisternal endoplasmic reticulum, a common feature of
transporting epithelial cells. In: Water Transport Across Epithelia. H.H. Ussing, N. Bindslev, and O. Sten-Knudsen, eds.
Munksgaard, Copenhagen, pp. 85–98.
Nadol, J.B. 1978 Intercellular junctions in the organ of Corti. Ann.
Otol., 87:70–80.
Nakazawa, K., S.S. Spicer, and B.A. Schulte 1995 Ultrastructural
localiation of Na,K-ATPase in the gerbil cochlea. J. Histochem.
Cytochem., 43:981–991.
Qvortrup, K., and J. Rostgaard 1990 Three-dimensional organization
of a transcellular tubulocisternal endoplasmic reticulum in epithelial cells of Reissner’s membrane in the guinea pig. Cell Tissue
Res., 261:287–299.
Rostgaard, J., and K. Møllgård 1980 Morphological evidence for a
transcellular pathway via elements of endoplasmic reticulum in
rat proximal tubules. In: Functional Ultrastructure of the Kidney.
A.B. Maunsbach, ed. Academic Press, London, pp. 251–266.
Salt, A.N., and T. Konishi 1986 The cochlear fluids: Perilymph and
endolymph. In: Neurobiology of Hearing: The Cochlea. R.A.
Altschuler, D.W. Hoffman, and R.P. Bobbin, eds. Raven Press,
New York, pp. 108–122.
Santos-Sacchi, J., and P. Dallos 1983 Intercellular communication in
the supporting cells of the organ of Corti. Hearing Res., 9:317–
Schmiedt, R.A. 1989 Spontaneous rates, thresholds, and tuning of
auditory nerve fibers: Comparison between cat and gerbil. Hearing Res., 42:22–36.
Schulte, B.A., and J.C. Adams 1989 Distribution of immunoreactive
Na1,K1-ATPase in the gerbil cochlea. J. Histochem. Cytochem.,
Schulte, B.A., and K.P. Steel 1994 Expression of a and b subunit
isoforms of Na,K-ATPase in the mouse inner ear and changes with
mutations at the Wv or Sld loci. Hearing Res., 78:65–76.
Spicer, S.S., and B.A. Schulte 1991 Differentiation of inner ear
fibrocytes according to their ion transport related activity. Hearing Res., 56:53–64.
Spicer, S.S., and B.A. Schulte 1993 Cytologic structures unique to
Deiters cells of the cochlea. Anat. Rec., 237:421–430.
Spicer, S.S., and B.A. Schulte 1994 Differences along the placefrequency map in the structure of supporting cells in the gerbil
cochlea. Hearing Res., 79:161–177.
Spicer, S.S., and B.A. Schulte 1996 The fine structure of spiral
ligament cells relates to ion return to the stria and varies with
place-frequency. Hearing Res. 100:80–100.
Spicer, S.S., and B.A. Schulte 1997 Evidence for a medial K1 recycling
pathway from inner hair cells. Hearing Res. (In press).
Sterkers, O., E. Ferrary, and C. Amiel 1988 Production of inner ear
fluids. Physiol. Rev., 68:1083–1128.
Tarnowski, B.I., R.A. Schmiedt, L.I. Hellstrom, F.S. Lee, and J.C.
Adams 1991 Age-related changes in cochleas of Mongolian gerbils.
Hearing Res. 54:123–134.
Voûte, C.L., K. Møllgård, and H.H. Ussing 1975 Qualitative relationship between active sodium transport, expansion of endoplasmic
reticulum and specialized vacuoles (‘‘scalloped sacs’’) in the outermost living cell layer of frog skin epithelium (Rana temporaria). J.
Membr. Biol., 21:273–289.
Wada, J., J. Kambayashi, D.C. Marcus, and R. Thalmann 1979
Vascular perfusion of the cochlea: Effect of potassium-free and
rubidium-substituted media. Arch. Otorhinolaryngol. Belg., 225:
Wangemann, P., J. Liu, and D.C. Marcus 1995 Ion transport mechanisms responsible for K1 secretion and the transepithelial voltage
across marginal cells of stria vascularis in vitro. Hearing Res.,
Без категории
Размер файла
1 450 Кб
Пожаловаться на содержимое документа