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Fertility and Spermatogenesis Are Altered in A1b-Adrenergic Receptor Knockout Male Mice

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Fertility and Spermatogenesis Are Altered in A1b-Adrenergic Receptor Knockout Male Mice 281 Fertility and spermatogenesis are altered in a1b-adrenergic receptor knockout male mice Sakina Mhaouty-Kodja, Anne Lozach, Rene´ Habert1, Magali Tanneux, Ce´line Guigon, Sylvie Brailly-Tabard2, Jean-Paul Maltier and Chantal Legrand-Maltier CNRS UMR 7079/Universite´ Pierre et Marie Curie, Neuroendocrinologie de la Reproduction, 4 Place Jussieu 75230 Paris CEDEX 05, France 1INSERM U566/CEA/Universite´ Paris 7, Unite´ Game´toge´ne`se et Ge´notoxicite´, DRR BP6, 92265 Fontenay-aux-Roses, France 2INSERM U135, Laboratoire d’Hormonologie et Biologie Mole´culaire, Hoˆpital de Biceˆtre, 94275 Le Kremlin Biceˆtre, France (Correspondence should be addressed to S Mhaouty-Kodja who is now at CNRS UMR 7148/Colle`ge de France, 11 place Marcelin Berthelot, 75231 Paris CEDEX 05, France; Email: [email protected]) Abstract To examine whether norepinephrine, through activation of that the mean absolute volume of Leydig cells per testis was not a1b-adrenergic receptor, regulates male fertility and testicular changed, suggests a compromised steroidogenic capacity of functions, we used a1b-adrenergic receptor knockout Leydig cells in infertile animals. In addition, RNA in situ (a1b-AR-KO) mice. In the adult stage (3–8 months), 73% of hybridization study indicated an apparent higher expression of thehomozygous maleswere hypofertilewithrelativelypreserved inhibin a-andbB-subunits in Sertoli cells of infertile spermatogenesis. Of the remaining males, 27% exhibited a a1b-AR-KO mice. This was correlated with a higher intra- complete infertility with a drastic reduction in testicular weight testicular content of inhibin B (C220% above wild-type mice). and spermatogenesis defect with germ cells entering a cell death Using specific primers, mRNA encoding a1b-AR was localized pathway at meiotic stage. In both phenotypes, circulating levels in early spermatocytes of wild-type testes. Our results indicate, of testosterone were highly reduced (K55 and K81% in for the first time, that a1b-AR signaling plays a critical role in the hypofertile and infertile males respectively versus wild-type control of male fertility, spermatogenesis, and steroidogenic males). Consequently,circulating levels of LH were significantly capacityof Leydig cells. It is thus hypothesized that the absence of elevated in a1b-AR-KO infertile mice. When incubated in vitro, a1b-AR alters either directly germ cells or indirectly Sertoli the whole testes from infertile KO mice released significantly cell/Leydig cell communications in infertile a1b-AR-KO mice. lower levels of testosterone (K40%). This, together with the fact Journal of Endocrinology (2007) 195, 281–292 Introduction Norepinephrine is implicated in a wide range of physiological processes through activation of nine different G-protein-coupled Noradrenergic innervation of the mammalian testis has been receptors (a1a, a1b, a1d, a2a, a2b, a2c, b1, b2, b3). In vitro studies shown by immunocytochemical and ultrastructural studies using selective adrenergic agonists or antagonists indicated that (Mayerhofer et al. 1999, Frungieri et al. 2000). Adrenergic both b-anda-adrenergic receptor (AR) might be involved in the nerve varicosities were located mainly in proximity of the neuroendocrine control of testicular functions (Ve rh oeven et al. Leydig cells, lamina propria of seminiferous tubules, and 1979, Cooke et al. 1982, Anakwe & Moger 1986, Mayerhofer et al. perivascular wall (Prince 1992, 1996), suggesting that the 1989, Wa n der ley et al.1989). However, whereas b1-/b2-subtypes norepinephrine released from sympathetic nerves has were shown to be predominantly expressed in Leydig and Sertoli multiple sites of action in the control of testicular functions. cells (To l s z c z u k et al. 1988, Eikvar et al. 1993, Troispoux et al. 1998, Disruption of the neuronal input (Chow et al. 2000), electrical Hellgren et al. 2000), the localization of a1-AR subtypes within stimulation of the spermatic nerves (Chiocchio et al. 1999) the testis is less documented and no data are presently available to as well as chemical sympathectomy with guanethidine assign functional role to specific a1-AR subtypes. (Rosa-e-Silva et al. 1995)or6-hydroxydopamine In recent years, much knowledge about the functions of (Mayerhofer et al. 1990) demonstrated that norepinephrine defined genes in spermatogenesis has been gained by making modulates luteinizing hormone (LH) receptors expression, use of mouse transgenic and gene knockout (KO) models. testosterone output, spermatogenesis, and testicular blood Indeed, spermatogenesis is under the complex control of flow. Interestingly, incubation of dispersed testicular cells with many molecular and cellular events. This involves gene norepinephrine or epinephrine significantly enhanced the expression in the developing germ cells, cell–cell interactions viability of spermatogenetic cells (Nagao 1989). of germ cells with Sertoli cells, communication between Journal of Endocrinology (2007) 195, 281–292 DOI: 10.1677/JOE-07-0071 0022–0795/07/0195–281 q 2007 Society for Endocrinology Printed in Great Britain Online version via http://www.endocrinology-journals.org Downloaded from Bioscientifica.com at 09/27/2021 08:39:36AM via free access 282 S MHAOUTY-KODJA and others . a1b-AR in mouse testicular functions tubular and Leydig cell compartments that are, in turn, of the mating period by evaluating spermatogenesis on testis regulated by gonadotropins and androgens (Skinner 1991, sections in comparison with wild-type animals. Saez & Lejeune 1996). Failure of any of these events leads to disturbances of male fertility. Therefore, to investigate the role Assay for mice genotyping of a1b-AR in testicular physiology, we used KO mice lacking the a1b-AR subtype (Cavalli et al. 1997). In the latter study, it Genotyping was performed by PCR using specific mouse was briefly reported that disruption of the a1b-AR gene does upstream and downstream primers of a1b-AR (Mhaouty-Kodja not seem to have any major effect on fertility since et al. 2001). The DNA was extracted from 1 cm tail-tip biopsy homozygous mice were capable of giving progeny and specimens of animals at 30-day post-natal byovernight incubation initiating the breeding colony. The present study was then at 55 8C in buffer (containing 100 mM Tris pH 8.5, 0.5% SDS, designed to determine more accurately the consequences of 0.2mMNaCl,5mMEDTA)withproteinaseK(100mg/ml). the a1b-AR-KO on male reproductive processes. For this After a phenol/chloroform extraction, genomic DNA contained purpose, we used appropriate experiments that addressed the in the supernatant was precipitated by the addition of 1 volume of effect of a1b-AR absence on testicular morphology, male isopropanol, washed twice with alcohol 70%, dried, and fertility and the level of gonadotropins, testosterone, and resuspended in sterile water. inhibin B in adult mice. The obtained findings underscore the role of a1b-AR signaling in the regulation of Leydig cell Reverse transcription (RT)-PCR analysis of a1b-AR expression homeostasis and spermatogenesis processes. Total RNAs from mice testis and liver were prepared using the RNA-PLUS kit (Bioprobe Systems, Montreuil, France). Five micrograms of total RNA were reversed-transcribed Materials and Methods using SuperScript Reverse Transcriptase kit from Gibco BRL Life Technologies and the resulting cDNA was stocked at Mice and tissue collection K80 8C. PCR was performed using specific mouse upstream The founder animals used to initiate our colony were wild- and downstream primers of a1b-AR (Mhaouty-Kodja et al. type (C/C) mice and a1b-AR-KO mice with 129/Sv! 2001) and the internal control hypoxanthine phosphoribo- C57BL/6J genetic background, kindly provided by Pr S syltransferase (Keller et al. 1993). The PCR products were Cotecchia (Cavalli et al. 1997). Adult males and females with separated by electrophoresis on an ethidium bromide- different genotypes and from different litters were randomly containing 2% agarose gel. Control PCRs performed on intercrossed to obtain a1b-AR C/C,C/K and K/K non-transcribed RNA indicated no contamination of the progeny. Only the resulting male a1b-AR-KO mice (K/K) RNA preparations with genomic DNA. and wild-type littermates (C/C) were used in the present experiments. Mice were housed in a room with a controlled Stereological analysis and immunohistochemistry photoperiod (lights on from 0900 to 1700 h) and temperature (22–24 8C) and were given free access to a nutritionally The left testis from each animal was fixed overnight by balanced diet (UAR B03) and water. Animals 3- to 8-month- immersion in Bouin’s fluid, after incision of the tunica old belonging to generations F2–F4 issued from the same albuginea. The fixed testes were divided into two along a colony were killed by cervical dislocation, in accordance with plane lying at right angles to the long axis. One half of each the guidelines for care and use of laboratory animals (NIH piece was dehydrated and embedded into methacrylate resin Guide). For hormone assays, blood was collected immediately (Technovit 7100; Kulzer and Co. Gmbh, Friedrichsdorf, by cardiac puncture and plasma was stored at K20 8C. Germany) according to the manufacturer’s instruction. Sections (3 mm) from each testis block were serially cut on a Reichert Jung 2050 (Nossloch, Germany) supercut micro- Fertility studies tome and then stained with toluidine blue. For the Continuous mating studies were performed during a quantitative assessment of the volumes of testicular compart- 2-month period to compare the fertility of the wild-type ments (seminiferous tubules, testis interstitium, Leydig cells), and a1b-AR-KO male mice. Three 12-week-old wild-type stereological methods were performed as previously described proven fertile females were allowed to mate with one male. using the point counting method (Kim et al. 2002). The Females were checked for post-coital plugs each morning. If a absolute volume of seminiferous tubules, interstitium, and plug was observed, the female was noted as being at day 1 of Leydig cells per testis was determined from the product of the gestation. Plug-positive females were killed on day 16 of volume fraction and the processed testicular volume.
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