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Department of Pathology and Laboratory Medicine, Brown University, Providence, Rhode Island 02912
Address all correspondence and requests for reprints to: Kamin J. Johnson, Department of Pathology and Laboratory Medicine, Brown University, Box G-B5, Providence, Rhode Island 02912. E-mail: kamin_johnson{at}brown.edu
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Abstract |
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, ß, and 
) were
found in testis. Using a semiquantitative RT-PCR assay, messenger RNA
expression was determined for each cadherin superfamily member during a
postnatal developmental time-course and following ablation of specific
testis cell types by ethanedimethanesulfonate, methoxyacetic acid, and
2,5-hexanedione. Diverse expression patterns were observed among the
cadherins, suggesting that cadherin expression is cell type-specific in
testis. The large number and variety of cadherin superfamily members
found in testis supports a critical function for cadherin-mediated
cell-cell adhesion in spermatogenesis. |
Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Members of the cadherin superfamily (cadherins) are critical components of adhesive interactions between cells (1, 3). Through homotypic interaction (in most instances) of their extracellular domains, cadherins physically link cells and provide spatial cues which modulate cell behavior. Cadherins convey this information by regulating intracellular signaling events via their cytoplasmic domains (1).
Classic cadherins and protocadherins are two subfamilies within the
cadherin superfamily (4, 5, 6). Both classic cadherins and protocadherins
share the typical cadherin repeats in their extracellular portion but
differ in their cytoplasmic regions. The cytoplasmic domain of classic
cadherins (both type I and II) contains conserved sequences that
interact with proteins termed catenins (7, 8). Recently, three families
within the protocadherin subfamily have been described: protocadherin
, ß, and (PCDH, ß and ) (6). PCDH and (and
likely ß) families are distinguished by unique cytoplasmic domains.
Within each PCDH family, individual members differ in their
extracellular domains but have identical cytoplasmic domains.
Therefore, each protocadherin family has the potential to mediate
numerous, unique cell-cell interactions but propagate specific
intracellular signaling events.
Examination of cadherin function in testis has been limited to classic cadherins. Munro and Blaschuk identified the expression of seven classic cadherins in mouse testis: E, N, P, K, T1, T2, and 11 (9). In vitro, adhesion between germ cells and Sertoli cells is mediated in part by N-cadherin (N-cad; 10, 11). These data are supported by N-cad immunostaining showing reactivity within the seminiferous epithelium and the presence of N-cad on both Sertoli cell and germ cell plasma membranes (10, 12, 13). Unlike N-cad, P-cad immunostaining in the adult testis is restricted to peritubular cells (14). E-cad immunostaining has not been demonstrated in the adult testis; however, it has been associated with various cell types in the developing and early postnatal mouse testis (15, 16).
Here, we used a degenerate PCR cloning and semiquantitative RT-PCR
strategy to investigate the expression of classic cadherins and
protocadherins in rat testis. A major result of this analysis was that
rat testis expressed at least 24 cadherins. Seven classic cadherins, 14
protocadherins, and 2 protocadherin-related cadherins were identified,
in addition to 1 cadherin-related receptor-like protein. Members of all
three protocadherin families (, ß, and ) were detected.
Analysis of messenger RNA (mRNA) levels of each cadherin during
postnatal development and following depletion of specific testis cell
types suggested that cadherins display unique, cell type-specific
expression.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Total RNA and complementary DNA (cDNA) preparations
cDNA was prepared from total RNA isolated using Tri Reagent
(Molecular Research Center, Inc., Cincinnati, OH),
according to the manufacturer’s protocol. For the cDNA reaction, 2
µg DNase-treated total RNA was primed with 3 µg random hexamers in
a total volume of 20 µl and cDNA extended using Superscript reverse
transcriptase according to the manufacturer’s protocol.
Detunicated testes from adult, toxicant-exposed, or postnatal days 7, 21, 28, and 40 rats were used to prepare total RNA. When testes from more than one animal were used, the tissue was pooled before isolating RNA. The number of animals used for each isolation were as follows: postnatal day 7 (8 rats), postnatal day 21 (4 rats), postnatal day 28 (3 rats), postnatal day 40 (2 rats). All other isolations were performed using one animal. In addition, total RNA was made from a Sertoli cell-enriched preparation isolated from 21-day-old rat testis using a standard protocol (17). For studies involving methoxyacetic acid (MAA; Aldrich Chemical Co., Inc. Milwaukee, WI), adult rats weighing 230 g were given a single dose of 650 mg/kg MAA by oral gavage (18). At days 3, 15, and 21 following MAA administration, rats were killed and total RNA prepared from one testis (weighing approximately 1.2 g at each timepoint). 2,5-Hexanedione (HD; Aldrich Chemical Co., Inc.) exposure was performed as previously described (19). After the characteristic atrophic state was achieved, total RNA was prepared from a single testis. For ethanedimethanesulfonate (EDS) treatment, an adult rat weighing 300 g was injected ip with 85 mg/kg EDS in 200 µl of 25% dimethylsulfoxide. Three days following EDS exposure, a testis weighing 1.25 g was used for isolation of total RNA. The three-day EDS timepoint was chosen since this gives near complete destruction of Leydig cells.
PCR cloning and screening
A degenerate PCR method similar to that of Suzuki et
al. (20) and Sano et al. (5) was used with slight
modifications. After an initial "hotstart" at 94 C, during which
RedTaq (Sigma, St. Louis, MO) was added, 35 PCR cycles
were performed using the following parameters: 94 C denaturation for
1.5 min, 45 C annealing for 2 min, and 72 C elongation for 3 min. As
PCR templates, randomly primed cDNAs made from total RNA isolated from
postnatal day 7 and adult rat testis were used (postnatal day 7 and
adult cDNAs were used in separate PCR reactions). All primers
(degenerate PCR cloning primers; Table 1
)
contained either EcoRI, HindIII, or
BamHI sites near their 5' ends to facilitate cloning of PCR
products into pBluescript II SK (Stratagene, La Jolla,
CA). For classic cadherins, degenerate primers against three regions of
the conserved cytoplasmic domain were used in two separate reactions to
increase the likelihood of detecting multiple cadherins. In the first
reaction, a forward primer (Classic Cadherin A) against the consensus
sequence GGGEED and a reverse primer (Classic Cadherin B) against the
consensus sequence PPYDSL were used; in the second reaction, the GGGEED
forward primer was coupled with a reverse primer (Classic Cadherin C)
against the consensus sequence FKKLAD. For PCDH family members, a
degenerate forward primer (PCDH A) against the consensus sequence
RDINDN located in the first extracellular domain and a degenerate
reverse primer (PCDH B) against the consensus sequence DGGKPE
located in the second extracellular domain were used. As general
primers for protocadherins, a degenerate forward primer (protocadherin
A) against the sequence
KP/GI/LDF/YE
and a degenerate reverse primer (protocadherin B) against the sequence
NDNAPX were used. These protocadherin primers are essentially those
used by Sano et al. (5), except for the addition of 5'
restriction sites.
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colonies. A potential cadherin clone showed a
colony PCR product of the expected size. The colony PCR product from
potential cadherin clones was used to sort these clones into similar
groups for DNA sequencing; groups were made by analyzing the
restriction pattern of colony PCR products following HinfI,
DdeI, or MseI digestion. DNA sequences of up to
four clones from each group were determined in cooperation with the
W. M. Keck DNA sequencing facility at Yale University.
Semiquantitative RT-PCR
A "primer-dropping" method (21) was used to determine the
expression of cadherin superfamily members relative to the housekeeping
gene hypoxanthine phosphoribosyltransferase (HPRT). During mouse
postnatal development, testis HPRT levels remain constant with respect
to ß-actin (22). In this method, two products of a multiplex PCR
reaction are kept in the linear range of amplification within the same
reaction by varying the cycle number at which one of the primer sets is
added. When a primer set (semiquantitative RT-PCR primers; Table 1
) was
added during PCR cycling, it was added during the denaturation step.
The following list details when the HRPT primer set was added during
cycling: FAT and PCDH-T2: HRPT added at the same cycle; Flamingo1a,
Flamingo1b, N-cad, PCDH4, PCDHC3, and PCDH-6: HRPT added after 2
cycles; PCDH3, PCDH8, PCDH11, and PCDH-T1: HPRT added after 3
cycles; PCDH-T5: HPRT added after 4 cycles; cad-10, PCDH9,
PCDH10, PCDH-T6, and VE cad-2: HRPT added after 5 cycles; PCDH-T3,
and PCDH-T4: HPRT added after 7 cycles; cad-11: HRPT added after 8
cycles; P-cad, E-cad, cad-6, and cad-8: HPRT added after 9 cycles.
For the PCR reaction using a Perkin-Elmer Corp. GeneAmp PCR System 2400 thermocycler, 1 µl cDNA was used as template in a 100 µl reaction containing 2.5 U RedTaq, cadherin and HPRT primer sets at 350 nM, 200 µM deoxyribonucleotides, and 1 x RedTaq PCR buffer. Ten-microliter samples were taken at the end of the elongation phase for seven consecutive cycles between cycle numbers 23–34, depending upon the primer set used. Cycle parameters were an initial 5 min, 94 C "hotstart" during which RedTaq was added followed by 30 sec, 94 C denaturation, 30 sec, 60 C annealing, and 30 sec, 72 C elongation steps. Cad-6 primers required a 53 C annealing temperature. The identity of PCR products was confirmed by restriction analysis (data not shown). Samples were electrophoresed on an agarose gel and visualized using ethidium bromide. TIFF images of the gels were made using Bio-Rad Laboratories, Inc. (Hercules, CA) Gel Doc 2000 gel imaging system; relative quantities of HRPT and cadherin PCR products were determined from the TIFF images using NIH Image 1.61. The data were represented as an average of two experiments. Error bars indicate the range of values of each primer set/template combination.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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) were designed to three conserved amino acid sequences found
in the cytoplasmic domain: GGGEED (classic cadherin A primer), PPYDSL
(classic cadherin B primer), and FKKLAD (classic cadherin C primer).
The GGGEED sequence was most conserved across known classic cadherins;
therefore, degenerate primers against this sequence were used in
combination with degenerate primers against PPYDSL or FKKLAD. The
classic cadherin A+B and A+C primer sets amplified products used for
cloning classic cadherins of approximately 230 bp and 360 bp,
respectively (data not shown).
Detection of PCDH family members was accomplished using degenerate
primers against the conserved RDINDN (PCDH A primer) and DGGKPE
(PCDH B primer) sequences found in the first and second cadherin
repeats of this family. PCR with PCDH A+B primers produced products
of approximately 310 bp (data not shown) used for cloning PCDH
family members. The final degenerate primer set (protocadherin A+B) was
intended to detect protocadherins without regard to their family
status. This primer set produced several bands following PCR (data not
shown), but the band at approximately 150 bp was selected for cloning
protocadherins (5).
Similar to brain, rat testis expressed a large number of cadherin
superfamily members. In total, 25 unique cadherin sequences were found:
7 classic cadherins of both types I and II, 14 protocadherins, 2
protocadherin-related cadherins, and 2 cadherin-related receptor-like
sequences (flamingo1a and b) (Table 2).
All known protocadherin families (, ß, and ) were expressed in
rat testis. Sequence analysis (described below) indicated that most, if
not all, protocadherin sequences represented unique proteins, not
different cadherin domains of the same protein; the greatest homology
was to the same cadherin repeat of different protocadherins. Of the
classic cadherins, the most frequent type isolated was N-cad, followed
by P-cad. Among the protocadherins and their related cadherins, VE
cad-2, and PCDH4 were the most frequent clones. Many cadherin
superfamily members were represented by only 1 clone. Unless we found a
striking homology to a protocadherin bearing an historical name, we
have chosen the nomenclature of Wu and Maniatis (6) for the
protocadherins described here. All sequences have been submitted
to GenBank (accession numbers AF177676-AF177700).
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A BLAST search using sequences of PCDH family members expressed in
rat testis indicated that rat testis expressed many of the same PCDH
proteins as did brain (6, 26). Homology at the nucleotide level between
the six PCDH sequences expressed in rat testis and human PCDH
genes ranged from a low of 76% identity (PCDH9) to a high of 84%
identity (PCDH3). The region we chose to amplify during PCR cloning
was not well-conserved among different PCDH family members (26). Our
rat testes PCDH clones showed high homology to only one PCDH
family member (data not shown). Therefore, it was likely that the rat
orthologs of human PCDH3, 4, 8, 9, 10, and 11 were expressed in
testis.
Because the protocadherin A+B primer set amplified a region well-conserved among protocadherins, many clones derived from this primer set showed equal homology to numerous protocadherins. In addition, the nonprimer-derived sequence was small for these clones (approximately 100 bp for most clones). Therefore, determining orthology with known protocadherins was difficult with clones from the protocadherin A+B primer set. Where no substantial (greater than 80% nucleotide identity) homology to a single gene existed without similar homology to other protocadherins, we chose a unique, temporary name for the clone.
We have identified six cadherin superfamily members from rat testis
that fit this description (PCDH-T1
T6). PCDH-T1 and -T2 were members
of the PCDH family. PCDH-T1 was most similar to PCDHA4, being
80% identical at the nucleotide level and 81% identical at the amino
acid level; the next highest degree of homology was with PCDHA12
(64% nucleotide and 66% amino acid identity). PCDH-T2 showed similar
homology to PCDHA9 and PCDHA10 at the nucleotide level (75% and
76% identity, respectively) and amino acid level (78% identity to
both PCDHA9 and PCDHA10). PCDH-T3, -T4, -T5, and -T6 were members
of the PCDHß family. T3 and T5 exhibited similar identity to rat
protocadherin-3 (27) at the nucleotide level (87% and 86%,
respectively; both have 81% identity at the amino acid level). T6 was
nearly identical to rat protocadherin-3: 95% nucleotide identity and
100% amino acid identity. Among the human PCDHß family members, T4
showed 76% nucleotide and 78% amino acid identity with PCDHß6.
The remaining rat testis clones identified using the protocadherin A+B
primer set were identical to previously cloned rat protocadherins or
were orthologs of cadherin superfamily members from other species. For
example, PCDHC3 was 100% identical to rat protocadherin-2
(accession no. AB004278) at the nucleotide and amino acid level and
shared 90% amino acid and 81% nucleotide identity to human PCDHC3.
Homology to other PCDH genes was much lower, so we suggest this is the
rat ortholog of human PCDHC3. Rat testis FAT and PCDH-6 shared 100%
nucleotide and amino acid identity to their previously cloned rat genes
(28; accession no. AB006802). Flamingo1a and flamingo1b clones were
homologous to two different cadherin domains in the mouse flamingo1
protein (29; accession no. AB028499). Although flamingo1 has
characteristics of a receptor protein (seven transmembrane-spanning
segments), it promotes homophilic cell aggregation (29). Flamingo1a was
truncated by an internal BamHI site and shared 100% amino
acid and 88% nucleotide identity to the third cadherin domain of mouse
flamingo1. Flamingo1b showed 100% amino acid and 90% nucleotide
identity to the sixth cadherin domain of mouse flamingo1. Finally, rat
testis VE cadherin-2 was likely the ortholog of mouse VE cadherin-2
(30), sharing 95% nucleotide and 100% amino acid identity.
Expression of cadherin superfamily members in rat testis
As a starting point to examine the biology of cadherin superfamily
members in rat testis, we explored their expression patterns during a
developmental time-course, following toxicant-induced ablation of
specific cell types, and in a Sertoli cell-enriched preparation (Figs. 1 and 2).
These experiments were designed to evaluate the cell type expression or
regulation of each cadherin.
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Type I and II classic cadherin mRNA expression in rat testis is shown
in Fig. 1A. Except for N-cad and cad-6, all classic cadherins were
expressed most abundantly at postnatal day 7. Compared with adult
testis, HD notably reduced the expression of E-cad, cad-6, and cad-10.
Elimination of Leydig cells by EDS dramatically reduced the expression
of cad-8 compared with adult levels; this was the only cadherin
superfamily member whose expression was reduced notably by elimination
of Leydig cells. Cad-8 expression also showed an increase in the adult
compared with postnatal day 40 testis. Elimination of significant
numbers of spermatocytes, round spermatids, or elongate spermatids by
MAA either increased expression of classic cadherins or had little or
no effect compared with adult levels. mRNA of all classic cadherins
were detected in a Sertoli cell-enriched preparation from 21-day-old
testis.
Like many of the classic cadherins, mRNA expression of PCDH and
PCDHß family members was greatest at postnatal day 7 (Fig. 1, B and
C). In general, expression levels were at a steady-state from postnatal
day 21 through adult for PCDH family members. However, expression of
PCDH3 was increased coincident with the presence of elongating
spermatids and dramatically reduced by HD-induced elimination of type B
spermatogonia and later germ cells. Except for PCHD9, PCDH-T3, and
PCDH-T6 where an increase in expression was observed, MAA
administration produced no remarkable consequences. Notable for the
PCDHß family was the observation that HD either increased their
expression or had no effect compared with adult testis. Expression of
PCDH and PCDHß family members was lower in the Sertoli
cell-enriched preparation compared with postnatal day 21.
The expression patterns of PCDH family members, flamingo1 clones,
and protocadherin-related cadherins FAT and VE cad-2 are shown in Fig. 2. As a group, the PCDH family members detected in testis displayed
varied expression patterns (Fig. 2A). While mRNA levels of PCDHC3
and PCDH-T1 were highest at postnatal day 7, PCDH-T2 and PCDH-6 were
highly expressed from postnatal day 40 through adult. Similarly, HD did
not decrease expression of PCDHC3 or PCDH-T1 but dramatically
reduced expression of PCDH-T2 and PCDH-6. Unlike most cadherin
superfamily members, PCDHC3 levels were relatively high in the
Sertoli cell-enriched preparation compared with postnatal day 21. The
expression patterns of the two flamingo1 clones (flamingo1a and 1b)
were notable for three reasons: their high expression at postnatal day
7, a striking reduction by HD, and a relatively high level in the
Sertoli cell-enriched preparation (Fig. 2B). FAT mRNA levels showed a
steady decline from postnatal day 7 through adult, were increased by
MAA exposure, and were relatively high in the Sertoli cell-enriched
preparation. VE cadherin-2 expression remained relatively constant
throughout postnatal development but declined in the adult testis; EDS
and MAA exposure raised its expression to levels observed during
postnatal development.
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Given the variety of cadherins expressed in testis, we hypothesize that cadherins will be found in all three junctions described above. It is also possible that cadherins will be localized outside of the morphological junctions described above, as is the case in other cell types (3). Experimental evidence suggest that cadherins mediate Sertoli-germ cell interactions. Study of testicular cadherins has focused on the classic cadherins. N-cad immunoreactivity has been observed associated with elongate spermatid heads, presumably ectoplasmic specializations, and other germ cell types (12, 13). In addition, connections resembling desmosome-like junctions and ectoplasmic specializations are detected between Sertoli and germ cells in vitro, and function-blocking N-cad antibodies partially inhibit Sertoli-germ cell interaction in vitro (10, 35, 36). Immunostaining and northern blotting both indicate that E-, N-, and P-cad are expressed in the developing and/or mature testis in unique patterns (12, 13, 14, 23, 37).
Using a similar strategy as that reported here, Munro and Blaschuk examined classic cadherin expression in the mouse testis (9). These authors found many of the same classic cadherins as reported here for rat testis, with a few exceptions. Expression of T1-cad and T2-cad was found in mouse testis while we did not detect either of these cadherins in rat testis. Likewise, we observed expression of cad-8 and cad-10 in rat testis while Munro and Blaschuk did not detect these cadherins in mouse testis. These differences are likely due to the use of different primer sets for degenerate PCR cloning and chance sampling events. K-cad was also reported to be expressed in mouse testis. However, comparing the reported K-cad sequence from mouse testis with rat testis cad-6 and rat K-cad indicates that mouse testis K-cad is cad-6, not K-cad. Our results argue that cad-6 and K-cad are closely related genes but not orthologs.
Although this report indicates that rat testis produces a great variety of cadherin superfamily members, it is likely that additional cadherins are expressed. Many cadherins were represented by only one clone following degenerate PCR, suggesting that our cloning survey was not saturating. Furthermore, additional cadherins have been reported in testis by others. A recently discovered type II classic cadherin, EY-cadherin, is detected in testis, brain, and eye (38).
Testis cadherin interactions might occur both heterotypically and
homotypically. Because most classic cadherins interact homotypically
(1), Sertoli cells and germ cells may express the same cadherin within
a given junctional complex. This view is supported by our expression
data showing that some cadherins (cad-10, PCDH3, PCDH-T2, and
PCDH-6) are highly expressed at postnatal day 7 but also greatly
diminished by HD exposure. One interpretation of this result is that
the postnatal day 7 expression is derived from Sertoli cells but that a
type B spermatogonium or later germ cell (killed by HD exposure) also
expresses the cadherin. The paradigm that Sertoli cells and germs cells
invariably express the same cadherin molecule at a given junction is
tempered by the morphological asymmetry of desmosome-gap junctions and
ectoplasmic specializations between Sertoli cells and germ cells (2).
This asymmetry suggests that Sertoli cells and germ cells potentially
produce unique cadherin molecules within each junction that can
interact heterotypically. Taken together, the data suggest that a
variety of homo- and heterotypic cadherin interactions likely exist
within the testis.
Our analysis of cadherin expression during postnatal development and following ablation of specific cell types by toxicant exposure suggests that each cadherin is produced in a subset of testicular cells. The current view of cadherin expression in brain is that each cell type produces a unique mosaic of cadherin superfamily members (39). We envision that all testis cell types express one or more cadherin superfamily members but that each cell type can be differentiated by its unique cadherin expression profile.
The scientific utility of a cell type-specific cadherin expression
pattern in testis would be great. The mosaic cadherin expression of a
particular cell could be used as a marker for that cell type.
Development of such markers would be beneficial for studying basic
testis biology as well as pathology and toxicology. Because cadherins
are integral plasma membrane proteins, isolation of viable, highly
purified testis cell populations would be possible using specific
antibodies and cell sorting. Table 3
describes potential markers for particular cell types. Our expression
analysis suggests that cad-8 is a potential marker for Leydig cells,
FAT and flamingo1 potential markers for Sertoli cells, cad-11 a
potential marker for an early germ cell type, and cad-6, PCDH3,
PCDH-T2, and PCDH-6 potential markers for type B spermatogonia or later
germ cells.
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In some instances (E-cad, cad-6, cad-10, PCDH9, PCDH-T3, FAT, and VE
cad-2), MAA exposure greatly increased cadherin expression compared
with adult levels. Syed and Hecht (40) have shown that MAA can alter
gene expression (negatively and positively) in both spermatocytes and
Sertoli cells; therefore, it seems that loss of specific germ cell
types following MAA exposure up-regulates the expression of many
cadherin superfamily members. This result implies that cadherin
expression is regulated by paracrine interactions within the
testis.
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Acknowledgments |
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Footnotes |
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Received September 1, 1999.
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N. P.Y. Lee, D. Mruk, W. M. Lee, and C. Y. Cheng Is the Cadherin/Catenin Complex a Functional Unit of Cell-Cell Actin-Based Adherens Junctions in the Rat Testis? Biol Reprod, February 1, 2003; 68(2): 489 - 508. [Abstract] [Full Text] [PDF]
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W.-Y. Lui, D. D. Mruk, W. M. Lee, and C. Y. Cheng Adherens Junction Dynamics in the Testis and Spermatogenesis J Androl, January 1, 2003; 24(1): 1 - 14. [Full Text] [PDF]
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 C. Y. Cheng and D. D. Mruk Cell Junction Dynamics in the Testis: Sertoli-Germ Cell Interactions and Male Contraceptive Development Physiol Rev, October 1, 2002; 82(4): 825 - 874. [Abstract] [Full Text] [PDF]
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P. Sluka, L. O'Donnell, and P. G. Stanton Stage-Specific Expression of Genes Associated with Rat Spermatogenesis: Characterization by Laser-Capture Microdissection and Real-Time Polymerase Chain Reaction Biol Reprod, September 1, 2002; 67(3): 820 - 828. [Abstract] [Full Text] [PDF]
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 X. Wang, H. Su, and A. Bradley Molecular mechanisms governing Pcdh-gamma gene expression: Evidence for a multiple promoter and cis-alternative splicing model Genes & Dev., August 1, 2002; 16(15): 1890 - 1905. [Abstract] [Full Text] [PDF]
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E. Hellsten, D. J. Bernard, J. W. Owens, M. Eckhaus, S. F. Suchy, and R. L. Nussbaum Sertoli Cell Vacuolization and Abnormal Germ Cell Adhesion in Mice Deficient in an Inositol Polyphosphate 5-Phosphatase Biol Reprod, May 1, 2002; 66(5): 1522 - 1530. [Abstract] [Full Text]
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K. J. Johnson and K. Boekelheide Dynamic Testicular Adhesion Junctions Are Immunologically Unique. I. Localization of p120 Catenin in Rat Testis Biol Reprod, April 1, 2002; 66(4): 983 - 991. [Abstract] [Full Text] [PDF]
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K. J. Johnson and K. Boekelheide Dynamic Testicular Adhesion Junctions Are Immunologically Unique. II. Localization of Classic Cadherins in Rat Testis Biol Reprod, April 1, 2002; 66(4): 992 - 1000. [Abstract] [Full Text] [PDF]
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 R.I. McLachlan, L. O'Donnell, S.J. Meachem, P.G. Stanton, D.M. de Kretser, K. Pratis, and D.M. Robertson Identification of Specific Sites of Hormonal Regulation in Spermatogenesis in Rats, Monkeys, and Man Recent Prog. Horm. Res., January 1, 2002; 57(1): 149 - 179. [Abstract] [Full Text] [PDF]
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D. J. Mulholland, S. Dedhar, and A. Wayne Vogl Rat Seminiferous Epithelium Contains a Unique Junction (Ectoplasmic Specialization) with Signaling Properties Both of Cell/Cell and Cell/Matrix Junctions Biol Reprod, January 1, 2001; 64(1): 396 - 407. [Abstract] [Full Text]
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 K. Boekelheide, S. L. Fleming, K. J. Johnson, S. R. Patel, and H. A. Schoenfeld Role of Sertoli Cells in Injury-Associated Testicular Germ Cell Apoptosis Experimental Biology and Medicine, November 1, 2000; 225(2): 105 - 115. [Abstract] [Full Text]
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