Expression of Mitotic Cyclin B1 is not Confined to Proliferating Cells in the Rat Testis1

Gromoll, Jörg; Wessels, Judith; Rosiepen, Giesa; Brinkworth, Martin H.; Weinbauer, Gerhard F.

doi:10.1095/biolreprod57.6.1312

Cited by 27 publications

(31 citation statements)

References 24 publications

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“…2). Our observation that some cell cycle genes are transcriptionally expressed at higher levels in purified round spermatids than in purified pachytene spermatocytes is consistent with previous reports (14). However, 18 of these genes were maximally expressed at stages XIII-XIV or stage I ( Table 3), indicating that their increased expression begins in spermatocytes.…”

Section: Analysis Of Defined Stages Of the Cycle Of The Seminiferous supporting

confidence: 92%

Stage-specific gene expression is a fundamental characteristic of rat spermatogenic cells and Sertoli cells

Johnston¹,

Wright

DiCandeloro³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

140

141

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Mammalian spermatogenesis is a complex biological process that occurs within a highly organized tissue, the seminiferous epithelium. The coordinated maturation of spermatogonia, spermatocytes, and spermatids suggests the existence of precise programs of gene expression in these cells and in their neighboring somatic Sertoli cells. The objective of this study was to identify the genes that execute these programs. Rat seminiferous tubules at stages I, II-III, IV-V, VI, VIIa,b, VIIc,d, VIII, IX-XI, XII, and XIII-XIV of the cycle were isolated by microdissection, whereas Sertoli cells, spermatogonia plus early spermatocytes, pachytene spermatocytes, and round spermatids were purified from enzymatically dispersed testes. Microarray analysis by using Rat Genome 230 2.0 arrays identified 16,971 probe sets that recognized testicular transcripts, and 398 of these were identified as testis-specific. Expression of 1,286 probe sets were found to differ at least 4-fold between two cell types and also across the stages of the cycle. Pathway and annotated cluster analyses of those probe sets predicted that entire biological pathways and processes are regulated cyclically in specific cells. Important among these are the cell cycle, DNA repair, and embryonic neuron development. Taken together, these data indicate that stage-regulated gene expression is a widespread and fundamental characteristic of spermatogenic cells and Sertoli cells.array analysis ͉ spermatogenesis ͉ seminiferous tubules ͉ stages of the cycle of the seminiferous epithellum ͉ contraception I n mammals, spermatogenesis encompasses a series of precisely timed cellular events that take place in a highly organized tissue, the seminiferous epithelium. Within each cross-section of this tissue, spermatogonia, spermatocytes, and spermatids are in intimate physical association with somatic Sertoli cells, and, together, these cells progress synchronously through the stages of the cycle of the seminiferous epithelium (1, 2). Four cycles are required for spermatogonia, and their progeny to complete spermatogenesis. The synchrony of germ cell development has a significant effect on the structures and functions of both the germ cells and their associated somatic Sertoli cells, suggesting the existence of precise and coordinated cyclic programs of gene expression. However, because investigators have evaluated the stage-dependent changes in expression of only a few genes, whether or not cyclic gene expression is a rare or prevalent characteristic of these cells is unknown (3-7). It is also not known whether genes encoding components of important biological pathways and processes are coordinately regulated in a cyclic manner. However, such genes may represent new targets for the development of male contraceptives.Given the coordinated nature of spermatogenesis, we hypothesized that the expression of large numbers of genes differ substantially, both between specific cell types within the seminiferous epithelium and within a given cell type as it progresses through the stages of...

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Section: Analysis Of Defined Stages Of the Cycle Of The Seminiferous supporting

confidence: 92%

Stage-specific gene expression is a fundamental characteristic of rat spermatogenic cells and Sertoli cells

Johnston¹,

Wright

DiCandeloro³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

140

141

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“…the cyclin B1 protein has been found to be expressed in postmeiotic spermatids and Sertoli cells but not in spermatogonia and spermatocytes (Gromoll et al, 1997), although no expression of cyclin B1 and B2 protein has been detected in the spermatids of mice testes (Brandeis et al, 1998). In medaka, a teleost fish, it has been reported that the cyclin B1 protein was expressed in spermatogonia and spermatocytes, except during the anaphase, whereas cyclin B2 was expressed in the same cells continuously (Mita et al, 2000).…”

Section: Discussionmentioning

confidence: 99%

Cloning of cDNAs and the differential expression of A‐type cyclins and Dmc1 during spermatogenesis in the Japanese eel, a teleost fish

Kajiura-Kobayashi

Kobayashi

Nagahama

2005

Developmental Dynamics

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We cloned A-type cyclins (cyclins A1 and A2) and Dmc1 cDNAs from the eel testis. Cyclin A1 mRNA was predominantly expressed in the livers, ovaries, and testes of the eels. In contrast to cyclin A1 mRNA, a very high expression of cyclin A2 mRNA was observed in the brains, livers, kidneys, spleens, ovaries, and testes of the eels. Dmc1 mRNA was predominantly expressed in the testes and ovaries; expression in the brain was also detected. In the eel testis, a few type-A spermatogonia incorporating 5-bromo-2 -deoxyuridine (BrdU) were seen before the initiation of spermatogenesis by hormonal induction. On day 1 after hormonal induction, the number of BrdU-labeled spermatogonia increased remarkably, and after 3 and 6 days, many labeled type-B spermatogonia were also observed. The expression of cyclin A2 increased 1 day after the induction of spermatogenesis and reached a plateau after 6 days, when many type-B spermatogonia with high proliferative activity were found. In contrast, the expression of cyclin A1 mRNA was detected after 9 days, coincident with the first appearance of spermatocytes. Cyclin A1 mRNA was localized in germ cells of all stages, from primary spermatocytes to round spermatids, whereas cyclin A2 mRNA was specifically localized in spermatogonia, secondary spermatocytes, round spermatids, and testicular somatic cells, including Sertoli cells. Dmc1 was localized only in the earlier stages of primary spermatocytes; before this stage, cyclin A1 mRNA was not detectable. Overall, cyclin A2, Dmc1, and cyclin A1 are expressed in spermatogenic cells sequentially before and during meiosis in the eel testis. Developmental Dynamics 232: 1115-1123, 2005.

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“…Exposure of rats to 14 days of ANT treatment induces a quantitative reduction of germ cell production but spermatogenic stages can still be recognized (Chandolia et al 1991b, Brinkworth et al 1995, Gromoll et al 1997. When extrapolated for the average time needed by a spermatogonium to develop into a mature testicular sperm, the difference is 1·2 days.…”

Section: Discussionmentioning

confidence: 99%

The cycle duration of the seminiferous epithelium remains unaltered during GnRH antagonist-induced testicular involution in rats and monkeys

Aslam¹,

Rosiepen²,

Krishnamurthy³

et al. 1999

Journal of Endocrinology

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Although the gonadotropic control of the spermatogenic process is well established, the endocrine regulation of the timing and kinetics of germ cell development has received little attention. We found previously that the administration of a GnRH antagonist (ANT) over a period of 25 days could retard spermatid development and slightly prolong cycle length in intact adult cynomolgus monkeys (Macaca fascicularis). The aim of the present study was to investigate the effects of extended exposure to ANT on the duration of the cycle of the seminiferous epithelium in the monkey. Additionally, the duration of spermatogenesis was studied in the ANT-exposed rat model. In experiment 1, monkeys were given either saline or ANT (n=6/group) and on day 30 all animals received a single injection of 5-bromodeoxyuridine (BrdU) to label S-phase germ cells. Testicular biopsies were taken on days 39, 43, 47 and 51 (end of treatment) for BrdU localization and flow cytometric analysis. ANT treatment suppressed hormone levels, reduced testis size by >70% and severely impaired germ cell production. Despite these alterations, cycle duration remained unchanged at all time-points compared with controls (10·12 0·15 days vs 10·16 0·44 days). In experiment 2, adult male Sprague-Dawley rats (n=15/group) received either vehicle (VEH) or ANT for 14 days and received BrdU injection on day 2. Cycle duration was found to be shorter in the ANT-treated group (12·45 0·09 days) than in the control group (12·75 0·08, P<0·05). As spermatogenic cycle length in this control group was longer than that of our historical controls (range: 12·37-12·53 days), experiment 2 was repeated (n=10/group). In experiment 3, cycle duration was 12·51 0·02 for VEH and 12·46 0·05 for the ANT-treated group (P>0·05) in both species. We concluded that the duration of the cycle of the seminiferous epithelium in monkeys and rats is independent of gonadotropins but is rather regulated by the spermatogenic tissue itself.

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Expression of Mitotic Cyclin B1 is not Confined to Proliferating Cells in the Rat Testis1

Cited by 27 publications

References 24 publications

Stage-specific gene expression is a fundamental characteristic of rat spermatogenic cells and Sertoli cells

Stage-specific gene expression is a fundamental characteristic of rat spermatogenic cells and Sertoli cells

Cloning of cDNAs and the differential expression of A‐type cyclins and Dmc1 during spermatogenesis in the Japanese eel, a teleost fish

The cycle duration of the seminiferous epithelium remains unaltered during GnRH antagonist-induced testicular involution in rats and monkeys

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