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Endocrinology Vol. 139, No. 1 350-357
Copyright © 1998 by The Endocrine Society

ARTICLES

The Localization of Messenger Ribonucleic Acids for Somatostatin Receptors 1, 2, and 3 in Rat Testis1

Li-Ji Zhu2, Krisztina Krempels2, C. Wayne Bardin3, Anne-Marie O’Carroll and Eva Mezey

The Population Council, Center for Biomedical Research (L.-J.Z., C.W.B.), New York, New York 10021; and Basic Neuroscience Program, National Institute of Neurological Disorders and Stroke (K.K., E.M.), and the Laboratory of Cellular and Molecular Regulation, National Institute of Mental Health (A.M.C.), National Institutes of Health, Bethesda, Maryland 20892

Address all correspondence and requests for reprints to: Dr. Li-Ji Zhu, The Population Council, Center for Biomedical Research, 1230 York Avenue, New York, New York 10021. E-mail: zhu{at}popcbr.rockefeller.edu


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Somatostatin (SRIF) exerts multiple inhibitory actions throughout the body by binding to specific SRIF receptors (sst). In recent years, five subtypes of SRIF receptors (sst1–5) have been cloned. In this study, 35S-labeled complementary RNA probes were used for in situ hybridization to localize the sst1–5 messenger RNAs (mRNAs) in the rat testis and examine the changes in their distribution during the cycle of the seminiferous epithelium. We found that sst 1–3 mRNAs were visualized in rat testes and were mainly localized within the seminiferous tubules. The signal for sst3 mRNA was also found in interstitial cells. sst4 and 5 mRNAs were not detected in rat testes with the method used in this study. In Sertoli cells, the most intense labeling for sst1 and 3 mRNAs was in stages IV–VII of the cycle of the seminiferous epithelium, which coincided with the lowest labeling intensity for sst2. In germ cells, sst1–3 mRNAs showed similar patterns of distribution. In these cells, sst1–3 mRNA was not observed at the early steps of spermatogenesis. Positive signals for sst1–3 mRNAs were first apparent in the pachytene spermatocytes at stage VII and last until stage XII and in the diplotene spermatocyte at stage XIII. Positive signals for sst1–3 were also detected in round spermatids at stages I–VIII. Labeling of spermatids dramatically decreased at stage IX, when these cells began their elongating changes. The presence of three sst in testis suggests that SRIF may play an essential role in testicular function.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
SOMATOSTATIN-14 (SRIF-14) and SRIF-28 are cyclic peptides that were first described as inhibitors of GH secretion from the pituitary (1). These peptides were subsequently demonstrated to exert a wide variety of inhibitory effects on endocrine, exocrine, and neural function in various organs (1, 2, 3, 4). The diverse biological actions of SRIF are mediated by multiple specific receptors (sst) that modulate adenylate cyclase, ion channels, and protein phosphatase activity (5, 6, 7, 8). Tissue targets of SRIF action were often in the same tissues as those in which this peptide was synthesized, suggesting that its actions were limited to autocrine or paracrine actions (2). In recent years, at least five SRIF receptors (sstl-5) were cloned from human and murine tissues (9, 10, 11, 12, 13). They belong to the superfamily of G protein-linked receptors that have seven membrane-spanning sequences (9, 11, 14). Northern blot analysis showed that the messenger RNAs (mRNAs) for these receptors are also widely distributed in various tissues and organs, including brain, pituitary, gut, pancreatic islets, heart, spleen, and kidney (9, 15, 16).

SRIF immunoreactivity was demonstrated in tissue extracts of the male reproductive system from human (17), boar (18), and rat (19). SRIF was also shown to modulate testicular steroidogenesis (20). These observations suggest that locally produced SRIF may exert autocrine and/or paracrine effects on testicular cells. As to our knowledge there was no information about the cellular localization of sst in testis, we thought it pertinent to gather such data. The purpose of the present paper was to determine the distribution of mRNAs of the five sst subtypes in adult rat testes by in situ hybridization using subtype-specific complementary RNA (cRNA) probes.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Six adult male Sprague-Dawley rats (Taconic Farms, Germantown, NY, 200–250 g) were decapitated. The testes were quickly removed, immediately frozen on dry ice, and stored at -80 C until sectioning. Twelve-micron thick sections were cut in a cryostat and mounted on silanized slides. The sections were dried on a warm plate (37 C) and then kept at -80 C until hybridization. Adjacent sections were hybridized to probes recognizing the five mRNAs encoding the different SRIF receptor subtypes (sst1–5).

The templates to make the riboprobes were as follows: sst1, bases 798-1429 (GenBank M97656); sst2, bases 1212–2003 (GenBank M93273); sst3, bases 2581–2980 and 1621–2277 (GenBank X63754); sst4, bases 1028–1464 (GenBank M96544); and sst5, bases 844-1644 (GenBank L04535) (21). 35S-Labeled antisense and sense riboprobes were prepared using the MAXIscript in vitro transcription kit (Ambion, Austin, TX). To ensure the specificity of the probes used in the hybridization, the second set of probes for different fragments of a same sst mRNA was prepared for each of the five ssts. sst1 (286 bp) and sst2 (565 bp) were generated by PCR from rat brain cortical complementary DNA. Primers for sst1 probe were 5'-CGC GCA ATT AAC CCT CAC TAA AGG TGC GGA GGA GCC TGT-3' and 5'-G CGC GTA ATA CGA CTC ACT ATA GGG CCT TAG TCA CAT AGC-3', and those for sst2 were 5'-CGC GCA ATT AAC CCT CAC TAA AGG TGG TCA AGG TGA GTG-3' and 5'-G CGC GTA ATA CGA CTC ACT ATA GGG CTA GCT ACT TGG GTT-3'. These specific upstream and downstream primers contained the T7 and T3 polymerase promoter regions, respectively. The PCR products were analyzed on a 1% agarose gel, gel purified, and then subcloned into the pNoTA/T7 vector using the Prime PCR Cloner Cloning System (5 Prime, 3 Prime, Boulder, CO). Templates for making sst1 and sst2 cRNA probes were generated by PCR reaction using the appropriate primers. The integrity of the sst1 and sst2 probes was later confirmed by DNA sequencing. The sst3 construct was subcloned into the pBluescript II KS+ vector and was described in detail previously. Primers for sst3 (313 bp) were 5'-CGC GCA ATT AAC CCT CAC TAA AGG TTC TCG GCG AGT ACG-3' and 5'-G CGC GTA ATA CGA CTC ACT ATA GGG CAG ATG GCT CAG CGT-3'. These upstream and downstream primers also included the T7 and T3 polymerase promoter regions at their 5'-ends, respectively. The integrity of this product was checked by restriction enzyme digestions. [35S]UTP-labeled antisense and sense riboprobes were prepared using the MAXIscript in vitro transcription kit.

In situ hybridization of the sections was carried out using these riboprobes as described previously (22). After overnight hybridization at 55 C, the sections were washed, air-dried, and exposed to Bio-MAX MR (Eastman Kodak, Rochester, NY) film for 3 days at room temperature. After the film was developed, the sections were coated with Kodak NTB3 emulsion and stored desiccated in the dark at 4 C for 28 days (except some slides for sst3 that were exposed for 10 days only). Then, the slides were developed in Kodak Dektol 19 at 15 C for 2.5 min, washed in distilled water, fixed with Kodak Fixer for 5 min, and counterstained with a 1% Giemsa stain. At each time, 60 series sections of testes from two animals were hybridized with antisense or sense probes for sst1–5 mRNAs. The experiments were repeated three times. Identical results were obtained in each experiment. Photographs were taken with a Nikon photomicroscope (Nikon Corp., Melville, NY) under darkfield and lightfield using x10 and x40 objectives. Images were recorded on Kodak TMAX-100 and Ektachrome 64T films.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Localization of sst1–5 mRNAs in rat testis
The mRNAs for three of the SRIF receptors (sst1, sst2, and sst3) were identified in frozen sections of rat testes as a high accumulation of silver grains in darkfield images (Fig. 1Go, A–D). The mRNAs for sst4 and sst5 were not detectable over the nonspecific background (Fig. 1Go, E and F). With the same hybridization procedure and same exposure time, sst1 and sst2 mRNAs showed comparable labeling intensities (Fig. 1Go, B and C) that were much less than the labeling for sst3 mRNA (Fig. 1DGo). In the sections hybridized for detection of sst1–3 mRNAs, the signals were variable in different tubules, suggesting that the accumulation of receptor mRNA could be dependent upon the stage of the seminiferous epithelium cycle. Labeling for sst1 and sst2 mRNA in the interstitial tissue was not consistent. Signal for sst3 mRNA was detected in more than half of the total interstitial cells, but the signal was much weaker than that in the seminiferous tubules (Fig. 1DGo, arrowheads).



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  		Figure 1. A and a are the lightfield photomicrograph corresponding to B and b, showing the structure of rat testis. Distribution of sst1–5 mRNAs in frozen sections of adult rat testis is shown in darkfield photomicrographs. Tissue sections from rat testes were hybridized with radiolabeled antisense probes for sst1 (B), sstr2 (C), sstr3 (D), sst4 (E), and sstr5 (F) mRNAs and exposed for 28 days. Sections hybridized with sense probes for sst1, sst2, and sst3 mRNAs are shown in b, c, and d. Arrowheads indicate interstitial cells. Magnification, x90. Bar = 100 µm.

 
A nonspecific background level distribution of silver grains was observed when adjacent sections were hybridized with sense probes (Fig. 1Go, a–d). In addition, sections hybridized with antisense probes for different fragments of a same sst mRNA displayed the same signal distribution and intensity. It was concluded that the hybridizations as performed in these experiments were specific for sst mRNAs.

Cyclic variation of sst3 mRNA in rat seminiferous epithelium
Frozen sections of rat testes hybridized with antisense probes for sst3 mRNA were exposed for a shorter period than those in Fig. 1DGo so that the cellular localization of sst3 mRNA could be determined. The high power darkfield and lightfield examinations (Fig. 2Go, A–D, a–d) indicated that the hybridization signals concentrated over the Sertoli cells and germ cells.



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  		Figure 2. Localization of sst3 mRNA in rat seminiferous epithelium by in situ hybridization (exposed for 10 days). A–D (darkfield) and a–d (lightfield) show the localization of sst3 mRNA in the Sertoli cells and germ cells in different stages of the seminiferous epithelium cycle, including stages I (A and a), V (B and b), VII (C and c), and XII (D and d). The stage of each high power lightfield photomicrograph is shown with a Roman number at the top. The following cells are indicated in the photomicrographs as follows: elongate spermatid (e), round spermatid (r), preleptotene spermatocyte (pl), zygotene spermatocyte (z), pachytene spermatocyte (p), and Sertoli cell (s). Magnification, x525. Bar = 20 µm.

 
Sertoli cells. The most intense labeling was observed in stages IV–VII, where the highest concentration of silver grains accumulated in the cytoplasm surrounding and overlapping the nuclei (Fig. 2Go, B, b, C, and c). The lowest intensity labeling was in stages XI–XIII, where silver grains were almost undetectable in some tubules (Fig. 2Go, D and d). The intensity of Sertoli cell labeling with sst3 antisense cRNA probes is shown diagrammatically in Fig. 4Go.



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  		Figure 4. Map summarizing the labeling for sst1 (A), sst2 (B), and sst3 (C) mRNAs in sections of rat testes hybridized with the antisense cRNA probes. The labeled cell types are crossed by bars that are defined by two lines. The height of the bars indicates the relative intensity of the signal in the cell along the length of the seminiferous tubule. The thicker lines used to describe the bars in C represent a much stronger labeling for sst3 mRNA than that of sst1 (A) and sst2 (B) mRNAs.

 
Spermatogonia. In contrast to Sertoli cells, the other cells in the basal compartment, type A and type B spermatogonia, did not show any positive signal for sst3 mRNA.

Spermatocytes. No distinct signals for sst3 mRNA were observed in the cytoplasm of the preleptotene (stages VII–VIII; Fig. 2Go, C and c), leptotene (stages IX–XI), or zygotene (stages XII–XIII; Fig. 2Go, D and d) spermatocytes. Similarly, no sst3 mRNA was detected in pachytene spermatocytes from stages XIV–V (Fig. 2Go, A, a, B, and b). Positive signals for this mRNA were first apparent in the cytoplasm of the pachytene spermatocytes in stage VII (Fig. 2Go, C and c) and progressively increased in the following stages until stage XII (Fig. 2Go, D and d) and, in the diplotene spermatocytes, stage XIII. The signal for sst3 mRNA decreased dramatically in stage XIV; it was almost undetectable in metaphase, anaphase, and telophase of meiosis I spermatocytes.

Spermatids. The labeling intensity present in the cytoplasm of round spermatids was similar in stages I–VIII (Fig. 2Go, A, a, B, b, C, and c). Signal for the mRNA began to decrease in stage IX when the round spermatids began their elongating changes and was undetectable in stage XII (Fig. 2Go, D and d) when the spermatids became elongated. No positive signals of sst3 mRNA was observed over the elongate spermatids in any subsequent stage of the cycle (Fig. 2Go, A, a, B, b, C, and c). The intensity of germ cell labeling with antisense probes for sst3 mRNAs is summarized in Fig. 4Go.

Cyclic variation of sst1 and sst2 mRNAs in rat seminiferous epithelium
Localization of sst1 and sst2 mRNAs was examined in sections after a long exposure time (28 days). Based on the observation of more than 200 tubules for each subtype of the SRIF receptors, both sst1 and sst2 mRNAs showed distributions similar to that of sst3 in germ cells. In germ cells, these mRNAs were highly expressed only in the late pachytene and diplotene primary spermatocytes and the round spermatids (Fig. 3Go, A–D and a–d). In the Sertoli cells, sst1 mRNA displayed a pattern of distribution similar to that of sst3 mRNA, as evidenced by a comparatively high expression in stages V–VII (Fig. 3Go, A and a). However, the pattern of distribution of sst2 mRNA was different, in that it was almost undetectable during stages V–X (Fig. 3Go, C and c) and began to appear at stages XI–XII (Fig. 3Go, D and d). The expressions of the three sst mRNAs are compared diagrammatically in Fig. 4Go.



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  		Figure 3. Localization of sst1 (A, a, B, and b) and sst2 (C, c, D, and d) mRNAs in rat seminiferous epithelium by in situ hybridization (exposed for 28 days; A–D, darkfield; a–d, lightfield). In germ cells, sst1 and sst2 mRNAs show similar distributions. The signals for both of them can be detected in late pachytene spermatocytes (B, b, D, and d; stage XII) and round spermatids (A, a, C, and c; stage V). In Sertoli cells, strong signals for sst1 mRNA can be found in stages V–VII (A and a; stage V), but the signal for ss2 mRNA is almost undetectable in these stages (C and c; stage V). The following cells are indicated in the photomicrograph as follows: elonate spermatids (e), round spermatid (r), zygotene spermatocyte (z), pachytene spermatocyte (p), and Sertoli cells (s). Magnification, x525. Bar = 20 µm.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
SRIF is synthesized from a common precursor as two bioactive forms, SRIF-14 and SRIF-28. The binding affinities of these two peptides to the five receptors is selective. In human tissue, the binding of SRIF-14 is relatively selective for sst1, -2, -3, and -4, whereas SRIF-28 is relatively selective for sst5. The only SRIF peptide demonstrated in rat testis by RIA and exclusion chromatography was SRIF-14 (19). These findings and our results are consistent with the postulate that SRIF-14 is a paracrine or autocrine regulator in rat testis.

Most previous studies on the distribution of sst in peripheral tissues were performed using Northern blot or nuclease protection assay (11, 15, 16), which could not demonstrate the cellular distribution within organs. The results of the present study with in situ hybridization histochemistry demonstrate that sst1, -2, and -3 mRNAs are distributed in Sertoli cells, late pachytene and diplotene spermatocytes, and round spermatids in some specific stages of the seminiferous epithelium cycle.

The present study demonstrates that sst1–3 mRNAs are detected in Sertoli cells, which suggests an effect of SRIF on Sertoli cell functions. All of the functions of Sertoli cells are regulated by FSH through its receptors that are coupled with adenylate cyclase through Gs proteins; cAMP activates protein kinase and results in the increased RNA expression and protein synthesis in Sertoli cell (23, 24, 25, 26). Testosterone, via its nuclear receptor, stimulates the synthesis of RNA and proteins in Sertoli cells and synergizes with FSH (26, 27). In contrast, in most cells after binding with SRIF, ssts are functionally linked to Gi protein, which leads to the inhibition of adenylate cyclase, a fall in intracellular cAMP, and a broad inhibition of cell function (10, 15, 28, 29). For example, SRIF inhibits gastric acid secretion, pancreatic enzyme secretion, GH release, and insulin release (30, 31, 32, 33). It is possible that SRIF will have a similar inhibitory action in Sertoli cells, which will be different from the actions of FSH. Previous studies indicated that the highest expression of FSH receptor mRNA in Sertoli cells is at stages XIV–II of the seminiferous epithelium cycle (34), and that of the testosterone (androgen) receptor is at stages VII–VIII (35). The results of the present study reveal that the highest accumulation of sst3 and sst1 mRNAs are at stages V–VII, just in between the peaks of FSH and androgen receptor mRNAs, respectively. Thus FSH, testosterone, and SRIF may act on different stages of the cycle to regulate Sertoli cell function during spermatogenesis.

In the present study, we also demonstrate the presence of sst1, sst2, and sst3 mRNAs in germ cells, which suggests a potential role for SRIF via its receptor on the regulation of germ cell development. The high accumulation of sst1–3 mRNAs in spermatocytes at stages VIII–XIII shown in this study suggest their potential involvement with germ cell meiosis. Further, the accumulation of sst1–3 mRNAs at a high level in round spermatides at stages I–VII and their dramatic decrease at stage IX when round spermatids began their elongating changes suggest some effects of SRIF and its receptors on spermiogenesis. In view of the inhibiting role of SRIF on most cells, it is possible that SRIF inhibits germ cell differentiation before meiosis and restrains the elongation of round spermatids until after mature spermatozoa are released from the epithelium at stage VIII.

A recent study showed that SRIF can alter testosterone secretion by Leydig cells (20). The present study demonstrates sst3 mRNA in most interstitial cells. If these cells express sst3 receptor, then it is possible that testosterone secretion can be regulated by SRIF with an autocrine or paracrine mechanism.


   Acknowledgments
 
We thank Ms. Jean Schweis for her assistance with the preparation of this manuscript.


   Footnotes
 
1 This work was supported in part by a grant from the NIH (HD-13541). Back

2 The first two authors contributed equally to this work. Back

3 Present address: National Institute of Child Health and Human Development, National Institutes of Health, Building 61E, Suite 8B01, Bethesda, Maryland 20892-7510. Back

Received May 20, 1997.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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