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Apoptosis in Epididymis of Sand Rat Psammomys Obesus

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Apoptosis in Epididymis of Sand Rat Psammomys Obesus +Model MORPHO-480; No. of Pages 11 ARTICLE IN PRESS Morphologie xxx (xxxx) xxx—xxx Disponible en ligne sur ScienceDirect www.sciencedirect.com ORIGINAL ARTICLE Apoptosis in epididymis of sand rat Psammomys obesus, Cretzschmar, 1828: Effects of seasonal variations, castration and efferent duct ligation L’apoptose dans l’épididyme du rat des sables itPsammomys obesus, Cretzschmar, 1828 : effets des variations saisonnières, castration et ligature des canaux efférents a,b,∗ c a,b a R. Menad , L. Lakabi , M. Fernini , S. Smaï , a d e T. Gernigon Spychalowicz , F. Khammar , X. Bonnet , f f E. Moudilou , J.M. Exbrayat a Small Vertebrates Reproduction, Laboratory of Research on Arid Areas, Faculty of Biological Sciences, Houari Boumediene University of Sciences and Technology, DZ-16111 El Alia, Algiers, Algeria b Cellular Pathology and Biotherapy, Laboratory for Valorization and Bioengineering of Natural Resources, Faculty of Sciences, Department of Natural and Life Sciences, University of Algiers, Algiers, Algeria c Production Laboratory, Protection of Endangered Species and Crops, Influence of Climatic Variations, Faculty of Biological Sciences and Agronomic Sciences, Mouloud Mammeri University, BP 15000, Tizi Ouzou, Algeria d Endocrine Ecophysiology of Reproduction in Saharan Mammals, Laboratory of Research on Arid Areas, Faculty of Biological Sciences, Houari Boumediene University of Sciences and Technology, El Alia, Algiers, Algeria e CEBC, UMR-7372 CNRS ULR, 79360 Villiers-en-Bois, France f Confluence Research Center—–Biosciences, Sciences and Humanities, Laboratory of Bioscience and Technology, Ethics, Lyon Catholic University, 10, place des archives, 69288 Lyon Cedex 02, France Received 16 July 2020 ; received in revised form 2 December 2020; accepted 20 December 2020 KEYWORDS Summary The aim of this study was to visualize apoptosis throughout the reproductive cycle Apostain; and after castration, castration then treatment with testosterone, and ligation of efferent ducts. The sand rat, Psammomys obesus, Cretzschmar 1828, is a diurnal rodent belonging to Cell death; ∗ Corresponding author: Cellular Pathology and Biotherapy, Laboratory for Valorization and Bioengineering of Natural Resources, Faculty of Sciences, Department of Natural and Life Sciences, University of Algiers, Algiers, Algeria. E-mail address: menadrafi[email protected] (R. Menad). https://doi.org/10.1016/j.morpho.2020.12.007 1286-0115/© 2020 Elsevier Masson SAS. All rights reserved. Please cite this article as: R. Menad, L. Lakabi, M. Fernini et al., Apoptosis in epididymis of sand rat Psam- momys obesus, Cretzschmar, 1828: Effects of seasonal variations, castration and efferent duct ligation, Morphologie, https://doi.org/10.1016/j.morpho.2020.12.007 +Model MORPHO-480; No. of Pages 11 ARTICLE IN PRESS R. Menad, L. Lakabi, M. Fernini et al. the family Gerbillidae. Its breeding cycle is seasonal with reproduction in autumn, winter and Season; early spring and a short resting period from late spring to early summer. Five groups of males Androgen were studied: (1) animals captured during the breeding season; (2) animals captured during the deprivation; resting season; (3) animals castrated and kept 30 days; (4) animals castrated, kept 30 days, Principal cells and then treated with testosterone for 15 days; (5) animals subjected to the ligation of effer- ent ducts and kept 30 days. Epididymis were removed and the presence of apoptotic cells was explored using the ‘‘Apostain’’ immunohistochemical method. Histological results showed cell and tissue remodeling. During the breeding season, a positive apoptotic signal was observed mainly in smooth muscle cells of caput and cauda epididymis. This signal persisted throughout the resting season. The orchiectomy induced apoptosis in almost of epithelial and connective cells. However, this intense cell death was not reversed by treatment with testosterone. In ani- mals that experienced efferent duct ligation, principal cells and smooth muscle cells showed a positive signal for apoptosis. Our results converge to qualify the sand rat epididymis as an excel- lent model for the study of apoptosis and argue for continued cell death, at least independent of circulating testosterone levels. © 2020 Elsevier Masson SAS. All rights reserved. Résumé L’objectif de cette étude est la mise en évidence de l’apoptose dans l’épididyme du rat des sables au cours du cycle de reproduction saisonnier et suite à des expérimentations, castration, castration puis traitement par testostérone et ligature des canaux efférents. Le modèle animal est le rat des sables, Psammomys obesus, Cretzschmar 1828, un rongeur déser- ticole diurne présentant un cycle de reproduction saisonnier avec une période d’activité de l’automne jusqu’au début du printemps, puis une période de repos sexuel limitée de la fin du printemps au début de l’été. Cinq lots ont été constitués; le premier et le deuxième concernent les animaux capturés en saison de reproduction et de repos sexuel respectivement. Le troisième et le quatrième correspondent respectivement aux groupes d’animaux castrés depuis 30 jours, et castrés depuis 30 jours puis traités pendant 15 jours à la testostérone. Le cinquième est le groupe d’animaux ayant subi la ligature des canaux efférents pendant 30 jours. Après sacrifice des animaux et prélèvement des épididymes proximaux et distaux, la recherche des cellules apoptotiques a été effectuée par la technique immunohistochimique Apostain. Pendant la sai- son de reproduction, un signal apoptotique positif est localisé principalement dans les cellules musculaires lisses de tête et la queue de l’épididyme. Cette apoptose persiste pendant la sai- son de repos sexuel. La castration induit une mort cellulaire concernant la plupart des cellules épithéliales et conjonctives tandis que le traitement des animaux castrés ne prévient pas cette dernière. Chez les animaux ligaturés, les cellules principales et les cellules musculaires lisses sont positives. Il semblerait que l’apoptose soit un processus continu indépendant de la durée de la castration et insensible à la testostérone. Malgré la diversité des éléments inducteurs de l’apoptose retrouvés chez les différentes espèces, l’épididyme du rat des sables semble constituer un très bon modèle pour l’étude de l’apoptose induite par la castration. © 2020 Elsevier Masson SAS. Tous droits reserv´ es.´ Introduction The sand rat, Psammomys obesus, Cretzschmar 1828 (Gerbillinae), is a diurnal desert rodent living in the Alge- rian Sahara. Reproduction is highly seasonal; breeding spans Many mammalian species, spanning from large ungulates from autumn to early spring and the resting period is lim- to small rodents, successfully adapted to the extremely ited to late spring — early summer. This species has been harsh environmental conditions that prevail in the most used to study various physiological adaptations and different arid deserts of the planet [1,2]. In response to strong metabolic disorders [5—9]. Investigations of seasonal varia- climatic and food availability variations, they developed tions of the reproductive system have shown cytological, various morpho-functional, ethological and physiological histological, biochemical and immunohistochemical remod- reproductive strategies. The seasonal reproduction cycles eling of the reproductive organs [8—19]. These results were of Gerbillinae (16 genera, 103 different species) provide consistent with seasonal hormonal fluctuations [20—24]. excellent examples of adaptive mechanisms that promote The epididymis is a key organ involved in post-gonadal parturition during the most favorable periods of the year sperm storage and maturation that exhibits cyclical struc- while large camelids rely on combined income and capital tural changes. Sperm maturation essentially depends on the breeding reproductive strategy to meet the demand of long quality of the environment offered to spermatozoa, the pregnancy and lactation [1—8]. 2 +Model MORPHO-480; No. of Pages 11 ARTICLE IN PRESS Morphologie xxx (xxxx) xxx—xxx composition of the epididymal fluid, entirely regulated by resting (June-July) seasons at Béni Abbès in the southwest epithelial cells with specific absorption and secretion func- of Algeria. After locating inhabited burrows thanks to the tions is thus crucial [25]. Previous studies have shown that presence of fresh tracks, traps were baited with small twigs the epididymis of Psammomys obesus is sensitive to seasonal of Chenopodiaceae. Adult males were captured very early in variations of androgens [16,26—28]. These steroids play a the morning. The animals were divided into 5 groups (Fig. 1): cascading role by triggering in the epithelial cells, the tran- scription and the translation of specific proteins secreted in • animals caught during the breeding season between Jan- the lumen that will affect the maturation of the spermato- uary and March (group 01, n = 10); zoa [29,30]. • animals caught during the resting season in June and July In the epididymis, androgens can act directly via andro- (group 02: n = 10). The three experimental groups were gen receptors (AR) or after conversion to DHT by 5␣ caught during the animals were the breeding season and reductase type I and II [31]. However, androgens can also subjected to specific treatments; exert their effect after irreversible conversion to 17␤ estra- • animals castrated and kept in captivity for 30 days diol by P450 aromatase [32]. Estradiol regulates essential (group 03: n = 8); epididymal functions, through binding to estrogen recep-
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