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From the * Department of Cell Biology, University
of Medical Sciences, Poznan, Poland; and the
Unit of Regulatory and Molecular Biology,
Departments of Cell Biology and Ophthalmology, SOM & NJMS, University of
Medicine and Dentistry of New Jersey, Stratford, New Jersey.
| Correspondence to: Anna Jankowska, ul. Swiecickiego 6, 60-781 Poznan, Poland (e-mail: ajanko{at}amp.edu.pl). |
| Received for publication April 6, 2006; accepted for publication August 16, 2006. |
 |
Abstract |
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 Top Abstract Materials and MethodsResults and DiscussionReferences |
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Key words: ROS-GC1, GCAP1, S100B, signal transduction
In the process of fertilization Ca2+ plays a key role. The
mechanisms controlling Ca2+ entry into the sperm, Ca2+
conductance, and ultimately the spermatozoa movement toward the oocyte, remain
unknown but are thought to involve various types of Ca2+ channels
(reviewed in: Benoff, 1998;
Publicover and Barratt, 1999;
Son et al, 2000; Jagannathan
et al,
2002a,b;
Castellano et al, 2003;
Chiarella et al, 2004;
Stamboulian et al, 2004;
Trevino et al, 2004). The
acrosomal activity of human spermatozoa is thought to be triggered by
Ca2+ influx mainly through 
1H T-type Ca2+
channels, expressed exclusively in spermatogenic cells
(Son et al, 2000; Jagannathan
et al,
2002a,b).
A novel Ca2+ channel, CatSper, present in the sperm has been cloned
(Nikpoor et al, 2004). This
gene encodes a unique and testes-specific Ca2+ channel. A
significant reduction in the level of CatSper gene expression has been
observed among patients with lowered sperm motility
(Nikpoor et al, 2004). Also a
cyclic nucleotide-gated channel has been identified in the mammalian sperm
(Weyand et al, 1994;
Wiesner et al, 1998). The
homooligomeric subunit cloned from bovine testes is roughly 200-fold
more sensitive to cyclic GMP then to cyclic AMP, suggesting that the channel
is specific and is a part of the cyclic GMP signaling pathway
(Wiesner et al, 1998).
Cyclic GMP is synthesized by a group of enzymes termed guanylate cyclases. Depending on their cellular distribution, these enzymes have been classified into 2 families, membrane-bound and soluble. The soluble form is heterodimeric in structure and is stimulated by nitric oxide and carbon dioxide (Murad, 1994; Middendorff et al, 1997; Pyriochou and Papapetropoulos, 2005). The membrane-bound form is a single transmembrane-spanning protein; it is monomeric, yet requires homodimerization for its activity (Chinkers and Wilson, 1992; Vaandrager et al, 1994; Wilson and Chinkers, 1995; Labrecque et al, 1999; Yu et al, 1999). On a biochemical basis, the membrane guanylate cyclase family is divided into 2 subfamilies, surface receptors and rod outer segment guanylate cyclase (ROS-GC). A central feature of the surface receptor subfamily is that all its members are receptors for peptide hormones or bacterial toxins (Fulle and Garbers, 1994; Leitman et al, 1994; Amin et al, 1996; Sharma and Duda, 1997; reviewed in: Sharma, 2002; Kuhn, 2003). These receptors, by binding their ligands, transduce the signal into production of the second messenger cyclic GMP.
The Ca2+-modulated membrane guanylate cyclase subfamily has been
named ROS-GC. ROS-GC subfamily is designed to transduce Ca2+
signals (reviewed in: Koch et al,
2002; Sharma,
2002; Sharma and Duda,
2006). ROS-GC machinery is a 2-component transduction system, the
enzyme ROS-GC and the Ca2+ sensor. It is expressed specifically in
the sensory and intermediary neurons of the retina
(Hayashi and Yamazaki, 1991;
Dizhoor et al, 1994;
Goraczniak et al, 1994;
Lowe et al, 1995;
Goraczniak et al, 1997),
pinealocytes (Venkataraman et al,
2000), the olfactory bulb (Duda et al,
2001a,b),
and the anterior portion of the gustatory epithelium
(Duda and Sharma, 2004). There
are 3 members of this subfamily, ROS-GC1, ROS-GC2, and ONE-GC, expressed
specifically in the olfactory neuroepithelium (Duda et al,
2001a,b).
These cyclases, in contrast to the peptide hormone receptor guanylate
cyclases, receive signals indirectly through Ca2+ sensor proteins,
which belong to 2 classes, guanylyl cyclase activating proteins (GCAPs) and
calcium dependent-GCAPs (CD-GCAPs). GCAPs receive the signals, undergo
conformational change and inhibit ROS-GC. CD-GCAPs receive the signals, also
undergo conformational change, and stimulate ROS-GC (reviewed in
Koch et al, 2002;
Sharma, 2002). GCAPs and
CD-GCAPs sense Ca2+ signals through their EF-hand domains. There
are 3 known functional GCAPs, 1, 2, and 3, and 2 CD-GCAPs, S100B and
neurocalcin 
(Palczewski et al,
1994; reviewed in Haeseleer et
al, 1999; Sharma,
2002; Sharma and Duda,
2006).
The presence and functional activity of the soluble and particulate (ANF-RGC and CNP-RGC) guanylate cyclase has been shown in testes (Marala and Sharma, 1988; Middendorff et al, 1996; Middendorff et al, 1997; Middendorff et al, 2000; Muller et al, 2004). In the sperm of marine invertebrates, the presence of chemotactic peptide receptors guanylate cyclases has also been shown (Ramarao and Garbers, 1985; Matsumoto et al, 2003), but there is no evidence of their presence in the mammalian sperm. Until now, the presence of Ca2+-modulated ROS-GC transduction system has been thought to be the exclusive domain of sensory or sensory-linked neuronal cells. This study documents the biochemical, molecular, and functional identity of a Ca2+-modulated membrane guanylate cyclase transduction machinery in bovine testes. The machinery is both inhibited and stimulated by free Ca2+ levels. The Ca2+-sensor component of the inhibitory mode of the machinery is GCAP1 and for the stimulatory mode is S100B. The transduction component is the guanylate cyclase ROS-GC1.
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Materials and Methods |
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TopAbstractMaterials and MethodsResults and DiscussionReferences |
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Antibodies
Characterization of highly specific antibodies raised against GCAP1, GCAP2,
S100B, and ROS-GC1 has been described previously
(Duda et al, 1998;
Venkataraman et al, 2000; Duda
et al,
2001a,b;
Duda and Sharma, 2004). The
antibodies were enriched by precipitating the immunoglobulin fraction using
ammonium sulphate. ELISA and Western blotting were used to test the
specificity and to determine the titer of purified antibodies.
Reverse Transcription Polymerase Chain Reaction
Bovine testes were purchased from a local slaughterhouse. The tunica
albuginea was removed, and total RNA was isolated from the fraction containing
seminiferous tubules and interstitial tissue using TriPure isolation reagent
(Roche Diagnostics, Mannheim, Germany) according to the manufacturer's
protocols. The cDNA library was constructed using Advantage RT for PCR kit
(BD-Biosciences, San Jose, Calif) and used for the amplification of the 548-bp
fragment of ROS-GC1, 373 bp of ROS-GC2, 627 bp of GCAP1, 601 bp of GCAP2, and
279 bp of S100B coding region. The amplified fragments were purified on
agarose gel and sequenced to confirm their identities. Additionally, as a
control, the 238-bp specific fragment of a housekeeping gene, large ribosomal
subunit (L30), was amplified from the cDNA library.
Preparation of the Membrane Fraction of Testes
Membrane fraction of bovine testes was isolated according to the protocol
described previously (Marala et al,
1991). The tissue fragments devoid of tunica albuginea, including
seminiferous tubules and interstitial tissue, were homogenized in a buffer
containing 250 mmol sucrose, 10 mmol Tris-HCl (pH 7.4), and 1 mmol
phenylmethylsulfonyl fluoride and centrifuged at 150 g for 10 minutes
to remove cell debris and nuclei. The post-mitochondrial supernatant (after
centrifugation at 400 x g and 10 000 x g) was
centrifuged at 40 000 x g. The pellet, designated as the
membrane fraction, was suspended in the homogenization buffer and stored at
–150°C until use.
Guanylate Cyclase Activity
The membrane fraction (
0.1 µg protein/sample) was assayed for
guanylate cyclase activity as described previously
(Paul et al, 1987;
Duda et al, 1998;
Venkataraman et al, 2000;
Duda and Sharma 2004).
Briefly, membranes were preincubated on an ice-bath with or without regulatory
proteins in the assay system containing 10 mmol theophylline, 15 mmol
phosphocreatine, 20 µg creatine kinase, and 50 mmol Tris-HCl, pH 7.5,
adjusted to appropriate free Ca2+ concentrations with precalibrated
Ca2+/EGTA solutions (Molecular Probes, Eugene, Ore). The total
assay volume was 25 µL. The reaction was initiated by the addition of the
substrate solution [4 mmol MgCl2 and 1 mmol GTP (final
concentrations)] and maintained by incubation at 37°C for 10 minutes. The
reaction was terminated by the addition of 225 µL of 50 mmol sodium acetate
buffer, pH 6.2, followed by heating in a boiling water bath for 3 minutes. The
amount of cyclic GMP formed was determined by radioimmunoassay
(Nambi et al, 1982). The RIA
system detects 2 fmol of cyclic GMP/sample.
Western Blotting
The procedure was carried out according to the previously published
protocols (Venkataraman et al,
2000; Duda and Sharma,
2004). Briefly, after boiling in gel-loading buffer (62.5 mmol
Tris-HCl [pH 7.5], 2% SDS, 5% glycerol, 1 mmol ß-mercaptoethanol, and
0.005% bromophenol blue) 150 µg of membrane protein was subjected to
SDS-PAGE in a buffer containing 0.025 mmol Tris-HCl (pH 8.3), 0.192 mol
glycine, and 0.1% SDS. The resolved proteins were transferred to
nitrocellulose membranes, and the blot was incubated in Tris-buffered saline
containing 0.05% Tween 20 (TBS-T), 5% powdered nonfat Carnation milk (blocking
buffer) overnight at 4°C. The anti-ROS-GC1, GCAP1, GCAP2, or S100B rabbit
polyclonal antibodies were added individually at dilution 1:1500, 1:1000,
1:1000, and 1:800, respectively. After 1 hour incubation the blot was rinsed
with TBS-T and the incubation was continued with the secondary antibodies
conjugated to horseradish peroxidase (1:10 000 dilution) in the blocking
buffer for another hour. Finally the blot was treated with SuperSignal blaze
chemiluminescent substrate (Pierce Biotechnology, Rockford, Ill) for 5 minutes
according to the manufacturer's protocol. The immunoreactive band was detected
by exposing the blot to Kodak X-ray film for 15 seconds. Images of the
membranes with the immunoreactive bands were acquired by scanning and
processed using Photoshop 6.0 software.
Immunohistochemistry
Paraffin sections of bovine testes fixed in 4% paraformaldehyde were used
for immunohistochemical detecting of ROS-GC1, GCAP1, and S100B. Antigens were
retrieved by microwave activation in citrate buffer (10 mmol, pH 6.0). After
being blocked in PBS containing 3% bovine serum albumin and 0.1% Tween 20,
sections were incubated with primary antibodies against ROS-GC1 diluted 1:200,
GCAP1 diluted 1:100, and S100B diluted 1:50 in the same solution for 60
minutes at 37°C in a humidified chamber and washed for 60 minutes in PBS
containing 0.1% Tween 20. AP-conjugated anti-rabbit IgG, diluted 1:200
(Sigma-Aldrich, Saint Louis, Mo) and NBT/BCIP as the substrate were used for
detection. Incubation and washing conditions were as described for primary
antibodies. Control included detection reactions carried out under identical
conditions, except that the primary antibodies were replaced by nonimmune
serum.
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Results and Discussion |
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TopAbstractMaterials and MethodsResults and DiscussionReferences |
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Testes Contain a Functional Ca2+-Dependent Membrane Guanylate Cyclase
Membrane fraction of bovine testes was isolated and tested for guanylate
cyclase activity. It was 3.5 pmol of cyclic GMP/mg protein/min. This is a
cumulative value representing all putative guanylate cyclases present in the
fraction. To assess whether the activity is Ca2+-modulated, the
membrane fraction was exposed to increasing concentrations of free
Ca2+ and the guanylate cyclase activity was measured. The results
(Figure 1A) show that the
fraction contained a guanylate cyclase, which was either stimulated or
inhibited depending on the free Ca2+ concentration. A range of
Ca2+ concentration from 10 nmol to 0.8 µmol caused a
dose-dependent decrease, and the higher range caused stimulation of the
membrane guanylate cyclase. The inhibitory IC50 value for
Ca2+ was 300 nmol, and the stimulatory EC50 value
was 5 µmol (Figure 1A).
These results show that the testes contain membrane guanylate cyclase, which
is both inhibited and stimulated by Ca2+ signals.
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(reviewed in
Koch et al, 2002;
Sharma and Duda, 2006). ONE-GC
is stimulated only by Ca2+-bound neurocalcin (Duda et al,
2001a,b;
Sharma and Duda, 2006).
To determine which 1 (or more) of these cyclases is expressed in the
testes, the membrane fraction of bovine testes was exposed to GCAP1, GCAP2, or
S100B in the presence of 10 nmol and 100 µmol Ca2+. The
stimulation by GCAP3 was not tested, since its expression was not detected in
bovine tissue (Haeseleer et al,
1999). In 10 nmol Ca2+ both GCAPs stimulated the
cyclase activity in a dose-dependent manner, with an EC50 of 1
µmol for GCAP1 and of 6 µmol for GCAP2
(Figure 1B). The maximal
stimulation of the cyclase was 2-fold above the basal value
(Figure 1B). There was no
stimulation by either GCAP in 100 µmol Ca2+
(Figure 1B). The
Ca2+-bound S100B also stimulated the cyclase activity in a
dose-dependent fashion (Figure
1C). The half-maximal stimulation was achieved at 0.8 µmol
S100B, and the maximal stimulation was 2.5-fold. Ca2+-free
S100B did not stimulate the cyclase activity
(Figure 1C). All these
stimulatory profiles are in accord with those established earlier for the
reconstituted systems consisting exclusively of recombinant ROS-GC1 and
individual Ca2+ sensor proteins, GCAP1, GCAP2, or S100B (Duda et
al,
1996a,b;
Duda et al, 1998;
Goraczniak et al, 1998;
Krishnan et al, 1998). The
ability of the cyclase to respond to both GCAPs (ROS-GC2 does not respond to
GCAP1) and S100B indicates that the membrane fraction of bovine testes
contains a guanylate cyclase that functionally mimics ROS-GC1
(Goraczniak et al, 1998;
Heaseleer et al, 1999). It is noted that the ability of exogenous GCAPs or
S100B (Figure 1B and C) to
stimulate ROS-GC1 in the testes membrane fraction beyond the point achieved
through only the removal or addition of Ca2+
(Figure 1A) indicates that
during the membrane preparation some Ca2+ sensor proteins were
lost; hence, their levels were lower than that necessary for maximal
activation of the cyclase.
The Transcript of ROS-GC1 Is Present in the Testes
To verify at molecular level the presence of ROS-GCs in bovine testes,
total RNA was isolated from the tissue, reverse transcribed, and a 548-bp
fragment corresponding to ROS-GC1 nucleotides 2042–2589 (GenBank
accession number P55203) and a 373-bp fragment matching to ROS-GC2 nucleotides
3276–3649 (GenBank accession number U95958) were amplified.
Amplification of a 238-bp fragment of the 30 kd ribosomal subunit (L30) served
as a control. In the cases of ROS-GC1 and L30, the amplification yielded
single bands of the predicted size (Figure
2A, lane 3, ROS-GC1; lane 4, L30). Sequencing of the amplified
ROS-GC1 fragment confirmed its identity with bovine ROS-G1. The amplification
of the ROS-GC2 fragment yielded no results
(Figure 2B, lane 2); however,
when cDNA from bovine retina was used as a control, the amplification yielded
a single band of the predicted size of 373 bp
(Figure 2B, lane 3). It is thus
concluded that the ROS-GC1 but not ROS-GC2 transcript is present in the bovine
testes.
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116 kd was observed in
control membranes (Figure 2C,
lane 1 and 2). A band of identical mobility was detected in the membrane
preparation from bovine testes (Figure
2C, lane 3). Identical results were obtained when antibodies
against the catalytic domain of membrane guanylate cyclase corresponding to
ROS-GC1 amino acid residues M872-S1016
(Fik-Rymarkiewicz et al, 2006)
were used in Western blots (data not shown). Thus through 3 independent
criteria, functional, molecular, and biochemical, it is concluded that the
sole ROS-GC expressed in the membrane fraction of bovine testes is
ROS-GC1.
Expression of GCAP1 and S100B in Bovine Testes
To determine whether GCAP1 and/or GCAP2 are responsible for the cyclase
stimulation in the absence of Ca2+
(Figure 1A; 10 nmol
Ca2+) and if S100B is responsible for the Ca2+-dependent
stimulation (Figure 1A;
0.8–100 µmol Ca2+), their presence was investigated at
both the RNA and protein levels. Using the specific primers designed based on
the known sequences of S100B (GenBank accession number DQ195377), GCAP1
(GenBank accession number X95352), and GCAP2 (GenBank accession number
U32856), RT-PCR was performed. A 279-bp fragment corresponding to the total
coding region of S100B and a 627-bp fragment corresponding to the total coding
region of GCAP1 were amplified (Figure
3A, lanes 2 and 3). Sequencing of the amplified fragments gave
exact match to bovine GCAP1 and S100B cDNAs. There was, however, no
amplification of a GCAP2 fragment (Figure
3A, lane 4). A single band of the predicted for GCAP2 size, 601
bp, was obtained in parallel control reaction with cDNA from bovine retina
(Figure 3A, lane 5).
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At the protein level, the identities of GCAPs and S100B in the membranes of
bovine testes were established by Western blot analysis using specific
antibodies against these proteins (Figure
3B). Anti-GCAP1 antibody detected a single band of apparent
mobility of 20 kd, identical to that of purified recombinant GCAP1 and
retinal membranes (Figure 3B,
panel "GCAP1&GCAP2," lanes 1, 2, and 3 for recombinant,
retinal, and testes, respectively). In agreement with the cDNA amplification
results, in testes membrane fraction there was no immunoreactivity with
anti-GCAP2 antibody (Figure 3B,
panel "GCAP1& GCAP2," lane 6). Anti-S100B antibody showed the
presence of 2 immunoreactive bands (Figure
3B, panel "S100B," lane 3). Bands of identical
mobility were observed for recombinant S100B and membranes isolated from
retina (Figure 3B, panel
"S100B," lanes 1 and 2). The mobility of these bands, 10 and
20 kd, corresponds to monomeric and dimeric forms of S100B. It is therefore
concluded that GCAP1, but not GCAP2, and S100B are expressed in bovine
testes.
ROS-GC1 Is Expressed in Germinal Cells of Bovine Testes
To determine the localization of the components of the ROS-GC1 transduction
system, immunohistochemical analyses were carried out with specific antibodies
against ROS-GC1, GCAP1, and S100B. In all specimens, the labeling was randomly
distributed in seminiferous tubules. The results are presented in
Figure 4. Staining for ROS-GC1
was observed predominantly in spermatogenic cells, especially in primary
spermatocytes and spermatids. However, single positively stained spermatogonia
were observed as well (Figure
4A). The increase in staining was detected across the cells in
different stages of the spermatogenesis process. The highest accumulation
visible in long spermatids appears to correlate with the stage of the
seminiferous cycle. The majority of spermatocytes and spermatids were stained
for S100B (Figure 4B). A
different pattern of immunostaining was observed with anti-GCAP1 antibody.
Only a small population of spermatogonia was stained for GCAP1
(Figure 4C). It can be
suggested that the expression of GCAP1 in these cells can be associated with
their biological activity. No labeling was observed in the controls, where the
primary antibodies were omitted (Figure
4D).
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The Ca2+ Modulated GCAP1/S100B - ROS-GC1 Signal Transduction Model
The present study, through functional, molecular, and biochemical
approaches, shows the presence of ROS-GC1 in the testes. The enzyme coexists
with its 2 Ca2+-dependent modulators, GCAP1 and S100B. In response
to localized changes in free calcium concentration, these proteins bind to the
specific domains, residing in the intracellular region of the cyclase, and
inhibit or stimulate ROS-GC1. In this manner Ca2+ pulses precisely
regulate the levels of cyclic GMP generated in 1 (or more) of the testes
cells. Given the presence of a cyclic GMP-gated channel in these cells, the
possibility exists that the levels control the hyper- or depolarized state of
those cells. This prediction opens up a new venue of research. And the finding
demonstrates that the presence of the ROS-GC transduction machinery is not
unique to the neurosensory and neurosensory-linked systems; it also exists in
the endocrinal system of the testes.
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Footnotes |
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