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From the * Department of Anatomy, University of
South Florida College of Medicine, Tampa, Florida; and
Department of Biomedical Engineering,
University of Florida, Gainesville, Florida.
| Correspondence to: Dr Katja M. Wolski, Department of Anatomy, University of South Florida College of Medicine, 12901 Bruce B. Downs Blvd, MDC6, Tampa, FL 33612-4799 (e-mail: kwolski{at}hsc.usf.edu). |
| Received for publication September 8, 2004; accepted for publication December 17, 2005. |
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Abstract |
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Key words: Ectoplasmic specialization, testis, micropipette, adherens junction
Several types of intercellular junctions, including occluding junctions, adherens junctions (AJ), and gap communicating junctions, are believed to play crucial roles in spermatogenesis. The actin based cell-cell AJs between the Sertoli cell and the germ cell in the mammalian testis are important not only in mechanical adhesion of the cells, but in the morphogenesis and differentiation of the germ cells (Russell, 1993). Turnover of these calcium-dependent junctions occurs during the process of germ cell migration from the basal to the adluminal epithelial compartment (Lui et al, 2003b).
The Sertoli ectoplasmic specialization (ES), a cytoskeletal structure of the Sertoli cell, is associated with Sertoli-spermatid binding at the AJ (Russell, 1977a, 1980). Abnormal or absent Sertoli ESs have been associated with a reduction of mature sperm in semen (Russell et al, 1988; Boekelheide et al, 1989; O'Donnell et al, 1996, 2000) and conditions associated with oligospermia (Cameron and Griffin, 1998). ESs are found basally in the Sertoli cell near Sertoli-Sertoli tight junctions and apically between Sertoli cells and spermatids. They consist of hexagonally packed bundles of actin filaments situated between the plasma membrane and a cistern of endoplasmic reticulum (Russell, 1993). The ES is an important cell-cell adhesion mechanism in the seminiferous epithelium to ensure the retention of spermatids as they mature into spermatozoa. ESs are first seen in the rat at Stage VIII of rat spermatogenesis, when the step-8 spermatid appears. It is thought the ES forms in the Sertoli cell to strongly anchor the step-8 spermatid to the seminiferous epithelium; however, this has yet to be actually measured. The ES is present at the AJ until appropriate release of the step-19 spermatid and inappropriate release of earlier stage spermatids (ie, spermatid sloughing) is related to abnormal ES structure and oligospermia (O'Donnell et al, 1996, 2000).
A number of health-related conditions are associated with reduced fertility potential and oligospermia in men, including varicocele, hyperprolactinemia, diabetes, and idiopathic oligospermia (Cameron and Griffin, 1998). These conditions all are associated with reduced sperm in the semen, that is, oligospermia, and ultrastructural pathology unique to the junctional apparatus of the seminiferous epithelium (Cameron and Griffin, 1998). Cap stage spermatids in the human (step-8 spermatids in the rat) are presumed to be tightly anchored to the seminiferous epithelium at a Sertoli cell AJ, which includes the unique Sertoli ectoplasmic specialization (Russell, 1977a, 1980). In both in vitro and in vivo observations of experimental animal models, disruption of this junction results in spermatid sloughing and subsequent oligospermia (Russell et al, 1988; Boekelheide et al, 1989; O'Donnell et al, 1996, 2000).
This project was designed to measure the strength of junctions between germ cells and Sertoli cells and to determine whether the presence of the unique ES between Sertoli cells and step-8 spermatids actually results in an increase in the binding strength between these 2 cell types. To do this, we have modified a micropipette pressure transducing system for the purpose of testing junctional strengths between cells in a Sertoli-germ cell coculture model optimized for cell-cell binding (Cameron and Muffly, 1991). It is hypothesized that the junctions between step-8 spermatids and Sertoli cells are stronger than those between pre-step-8 spermatids and Sertoli cells and between spermatocytes and Sertoli cells.
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Materials and Methods |
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Sertoli Cell Isolation, Culture, and Pretreatment
Briefly, testes were excised from prepubertal male rats, and the parenchyma
was digested using routine sequential enzymatic treatments with trypsin
(0.25%, Sigma Chemical Co, St Louis, Mo) and collagenase (0.20%, Becton
Dickinson, Sparks, Md). Isolated cells were plated to confluence on 13-mm
round plastic coverslips coated with undiluted Matrigel in 24-well cell
culture dishes. Cultures were incubated in Dulbecco's Modified Eagle Medium:
Nutrient Mixture F12 (Ham) (DMEM:F12) (supplemented with 0.01 mol/L retinol
and 1000 µL/100 mL insulin-transferrin-selenium [ITS]) at 39°C in a
humidified incubator with 5% CO2-95% air for 48 hours to expedite
the removal of contaminating germ cells. After the 48-hour preincubation, the
cultures were exposed to a 20 mM Tris-HCl buffer for 2.5 minutes to
hypotonically lyse remaining germ cells, then incubated in supplemented
DMEM:F12 at 33°C in a humidified incubator with 5% CO2-95% air
for 24 hours. After the 24-hour incubation, the media were replaced with
supplemented DMEM:F12 containing 0.06 µg/mL follicle-stimulating hormone
(FSH) (NIDDK-oFSH-20, AFP7028D, 175xNIH-FSH-S1) and 100 nM testosterone
(Sigma). These pretreated Sertoli cell cultures were used in all coculture
experiments.
Spermatocyte and Round Spermatid Isolation and Unit Gravity Velocity Sedimentation
Spermatocytes and pre-step-9 spermatids (round spermatids) were isolated
from an adult male rat testis. Briefly, the decapsulated adult testis was
digested with 0.10% collagenase (Gibco, Carlsbad, Calif; 37°C, 80
oscillations/min, 30 minutes) to separate seminiferous tubules from the
testicular interstitial tissue. The washed seminiferous tubules then were
digested with 0.25% trypsin (Sigma; 37°C, 90 oscillations/min, 15 minutes)
to separate the peritubular cells from the seminiferous epithelium and to
expedite the release of germ cells from the seminiferous epithelium. A 0.20%
trypsin inhibitor solution (Sigma) was added to terminate the trypsin
reaction. The resulting cell suspension (mixed germ cells and Sertoli cells)
was resuspended in 25 mL McCoy media plus 0.5% bovine serum albumin (BSA).
With sterile technique, the gradient chambers on a STA-PUT velocity sedimentation cell separator were filled with the appropriate McCoy media plus BSA medium (2% and 4% BSA), and a linear gradient (2%-4%) was built under the cell suspension, at the loading rate initially at 10 mL/min. After 20 minutes, the rate was increased to 40 mL/min. Eighty minutes before the end of the collection time (4 hours), media with germ cell fractions were collected using a Fractomat automatic fraction collector (10 mL/vial at 160 drops/min). Spermatocytes and round spermatids (pre-step-9) were identified by phase contrast microscopy and pooled, washed, and resuspended in McCoy media. The number of cells in the spermatocyte and spermatid fractions were counted by hemocytometric analysis and assayed for viability by trypan blue exclusion.
Sertoli-Germ Cell Coculture
Approximately 400 000 isolated germ cells (spermatocytes and round
spermatids) were added directly to the pretreated Sertoli cell-enriched
monocultures. The Sertoli-germ cell cocultures were incubated with 0.06
µg/mL FSH plus 100 nM testosterone in a humidified chamber at 33°C with
5% CO2-95% air for 36 hours.
Measurement of Junctional Strength Using a Micropipette Pressure Transducing System
The Sertoli-germ cell cocultures were imaged on an inverted interference
contrast microscope (Axiovert 100, Zeiss, Germany) with a 20x objective.
The microscope was fitted with the micropipette pressure transducing system
(MPTS), which consisted of a 3-dimensional water robot micromanipulator
(Narishige Scientific Instruments Lab, Tokyo, Japan), a micropipette holder, a
glass micropipette, a water reservoir system to control the micropipette
pressure, and a video system to record experiments
(Figure 1).
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The Micropipette
Micropipettes were created from 1-mm outer diameter, 0.5-mm inner diameter
glass capillary tubes (A-M Systems Inc, Carlsbad, Wash). The capillary tube
was mounted onto a pipette puller (model PB-7, Narishige Scientific
Instruments), heated, and pulled into a pipette with a tip of a few microns.
To ensure a flat tip, this pipette was then mounted onto a microforge (model
MF 83, Narishige Scientific Instruments). The microforge consists of a
horizontal microscope, a micromanipulator, and a glass bead on a platinum
wire. Upon heating of the wire, the glass bead melted and the tip of the
micropipette was inserted into the melted glass. The bead/micropipette was
allowed to cool. The micropipette was then pulled up, and the tip was broken
by quick fracture, leaving a flat tip. The tip was filled with a saline
solution to avoid plugging. To prevent rupture of the cells on the glass
surface, the micropipette was coated with plasma proteins. The diameters of
the pipettes used were 13.32 µm for spermatids (diameter 10 µm) and
16.65 µm for spermatocytes (diameter 15 µm).
The Water Reservoir System
The pressure at the tip of the micropipette was controlled by a system
consisting of 2 water reservoirs and a pressure transducer (model DP15-30,
Validyne, Northridge, Calif) connected between the 2 reservoirs. One reservoir
was a reference reservoir, and the other one was an adjustable reservoir. The
reference reservoir was adjusted so that no pressure would be applied at the
micropipette. This was achieved by connecting the reference reservoir directly
to the micropipette and positioning it at the same level as the micropipette.
As a result, there were no movements from particles or cells in front of the
micropipette. The adjustable reservoir was then positioned to create the
desired pressure, as read by the pressure transducer. A valve switch was used
to connect the micropipette either to the reference reservoir or the
adjustable reservoir. The pressure transducer output signal was decoded via a
carrier demodulator (model CD 280-2, Validyne). The pressure range of the
transducer was 80 000 dyn/cm2 with an accuracy of 400
dyn/cm2.
Cell Measurements
Cover slips containing Sertoli-germ cell cocultures were carefully removed
from the wells and placed in an engineered cover slip holder for use with the
MPTS-fitted inverted microscope. The detachment of germ cells from Sertoli
cells was measured and analyzed. In some experiments, 2 mM or 4 mM EDTA was
added to the cultures immediately before the measurements, as controls. To
detach germ cells from Sertoli cells, the micropipette was brought to the
surface of the individual spermatocyte or the individual spermatid at
200x magnification making sure not to touch the underlying Sertoli
cells. If the Sertoli cells were touched by the micropipette, the measurement
was abandoned. The pressure required to detach the germ cell from the
underlying Sertoli cell monolayer was then recorded. Each detachment event (a
maximum of 4) consisted of a 5-second suction pressure interval. If the germ
cell did not dissociate, it was abandoned, and the last pressure reading was
recorded. The recorded pressure (in cm-H2O) was used to calculate
force via the equation F = 
P x
R2p, where F (pN) is the force on a
static cell, P is the suction pressure (N/µm2),
and R2p is the cross-sectional area of the
pipette (µm2). To convert the pressure reading received in
cm-H2O to N/µm2, for use in the above equation, the
conversion factors 1 cm-H2O = 98.06 Pa and 1 Pa = N/m2
were used, since the international unit of force is Newtons (1 N = 1 kg
m/s2), and the international unit of pressure is Pascal (Pa).
Statistics
To determine statistical significance of the mean force (set at the 0.05
level), a 1-way analysis of variance (ANOVA) was performed, followed by
Tukey's honestly significant difference test.
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Results |
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A 1-way ANOVA determined a significant difference between the mean force of spermatocytes and the mean force of step-8 spermatids, between the mean force of pre-step-8 spermatids and the mean force of step-8 spermatids, and between the mean force of spermatids versus spermatids plus EDTA, where P < .05. There was no significant difference between the mean force of spermatocytes and the mean force of pre-step-8 spermatids.
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Discussion |
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TopAbstractMaterials and MethodsResultsDiscussionReferences |
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We have, for the first time, recorded actual force measurements necessary to detach germ cells from underlying Sertoli cells in vitro. The results suggest that the force measurements are related to the junctional strength between the various germ cell types and the Sertoli cells in a manner consistent with well-established theories related to germ cell-Sertoli cell attachments. On this basis, the data presented confirm the hypothesis that step-8 spermatids are more firmly attached to Sertoli cells than are pre-step-8 spermatids and spermatocytes. It is possible that the force recorded represents the membrane stability of just the germ cell type and not the actual strength of the junctional structure. More studies are needed to make this determination, but in either case, it was clearly more difficult to detach step-8 spermatids from Sertoli cells than the other germ cell types tested.
Of the cells tested, the ES is only present between Sertoli cells and step-8-step-19 spermatids and is conspicuously absent between Sertoli cells and spermatocytes and pre-step-8 spermatids (Russell, 1993). This suggests that the structural nature of the ES contributes to the actual junctional strength between these 2 cell types, ensuring that elongating spermatids (post-step-8 spermatids) are securely anchored to the seminiferous epithelium during the final stages of spermiogenesis. This also supports the hypothesis that when the ES does not form properly between the Sertoli cell and the periluminal step-8 spermatid, or is otherwise abnormal, the junction strength is significantly lessened, thereby leading to spermatid sloughing and oligospermia (Cameron and Griffin, 1998).
Several molecular models of the structure and regulation of the ectoplasmic
specialization at the Sertoli cell-spermatid junction have been proposed. One
such model includes the controversial and most studied cadherin-catenin
complex. In this model, it is proposed that the presence and regulation of the
multiprotein cadherin-catenin complex at the ES controls the coupling and
uncoupling of spermatids to Sertoli cells
(Newton et al, 1993;
Wine and Chapin, 1999;
Lee et al, 2003). Disruption
of this protein complex via phosphorylation of p120ctn
(Daniel and Reynolds, 1997), tyrosine phosphorylation of ß- and/or 
-catenin
(Daniel and Reynolds, 1997),
and/or the addition of an anti-N-cadherin antibody
(Newton et al, 1993;
Perryman et al, 1996) results
in the loss of germ cells from the seminiferous epithelium. This step-8
sloughing, as described by O'Donnell et al
(1996), is also related to
testosterone reduction and possibly, therefore, N-cadherin expression
(Newton et al, 1993;
McLachlan et al, 1994;
O'Donnell et al, 1994). In
vitro, testosterone and dihydrotestosterone with a fixed concentration of FSH
causes a dose-related increase in N-cadherin levels
(Perryman et al, 1996).
Increasing doses of FSH in the presence of a fixed concentration of
testosterone also creates a dose-related increase in N-cadherin protein levels
(Perryman et al, 1996). In the
models studied, the ES is still present, indicating that testosterone has an
effect on the cell adhesion molecules at this junction and not the ES
structure itself (McLachlan et al,
1994; O'Donnell et al,
1994,
2000). The effects of
reproductive hormones on cell adhesion and coupling and uncoupling dynamics
between Sertoli cells and germ cells, as defined above, can be tested using
the MPTS.
Other proposed molecular models of the Sertoli-spermatid ES consist of the nectin-afadin-ponsin complex and the integrin complex. Nectins are found in both Sertoli cells (nectin-2) and spermatids (nectin-3), with the strongest expression at stages IV-IX and decreasing at stage VIII (Bouchard et al, 2000; Ozaki-Kuroda et al, 2002). 1-Afadin, found in the testis, connects to the actin cytoskeleton (Mandai et al, 1997), and studies using afadin-/- mice have shown that afadin is essential in proper structural organization of tight junctions and cadherin-based AJs (Ikeda et al, 1999). Ponsin, of which mRNA is found in the testis (Mruk and Cheng, 2004), binds to afadin and allows it to colocalize with nectin to the cadherin-based AJ (Mandai et al, 1997). However, no biochemical or functional studies on the nectin-afadin-ponsin complex have been conducted.
The most studied integrin receptor in the testis is 
6ß1, which
is found in the Sertoli cell membrane (for review,
Vogl et al, 2000). The binding
partner of 6ß1 is not yet known, but recent studies have indicated
that the laminin 3 chain is a putative binding partner
(Koch et al, 1999;
Mulholland et al, 2001; Siu and Cheng, 2004). The
expression of ß1-integrin has been shown to be affected by hormones.
Testosterone, in the presence of FSH, increases ß1-integrin levels in a
dose-dependent manner (Pearce,
2003), as do increasing doses of FSH in the presence of
testosterone. Integrins are important in cell adhesion not only structurally,
but also in that they transmit signals to trigger events that activate signal
transducers, such as Rho GTPase (Lui et
al, 2003a), focal adhesion kinase
(Mulholland et al, 2001;
Siu et al, 2003), Src
(Wine and Chapin, 1999),
C-terminal Src kinase (Wine and Chapin,
1999), and integrin-linked kinase
(Mulholland et al, 2001), to
affect Sertoli-germ cell AJ dynamics (Lui
et al, 2003b). Again, the effects of reproductive hormones on the
integrin-based model of the Sertoli-germ cell junction and its role in
coupling and uncoupling of germ cells from Sertoli cells can be tested with
the MPTS.
Results from this study show that the junctional strength between Sertoli cells and germ cells can be measured in vitro, support long-held speculations regarding Sertoli-spermatid junctional interactions, and provide a means to actually test proposed mechanisms of junction dynamics between cells of the seminiferous epithelium.
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