Mammalian testis undergoes deep changes in their architecture and function during photoregression conditions in seasonal breeders. Particularly, the testicular mechanisms that regulate the transition between the active (functional) and inactive (regression) stage vary between species. The aim of the present study was to analyze the incidence of proliferation, apoptosis and autophagy in the testicular seminiferous ephitelium of a seasonal breeder, Lagostomus maximus, during the annual reproductive cycle. We observed that proliferating spermatogonia increased from the active testis until reaching the maximum peak in the activating testis. During the annual reproductive cycle, the quantity of apoptotic-TUNEL positive spermatogonia and meiotic germ cells was constant and this might be regulated by the members of the BCL2 family. Only in the activating testis, apoptosis of germ cells was almost undetectable. The analysis of the autophagic-related proteins BECN1 and LC3 showed their localization in Leydig cells and the germ cells in the active and activating testis. In the inactive testis, BECN1 and LC3 ceased to be immunolocalized within the seminiferous tubules and the mRNA expression of both regulators decreased. Moreover, the expression of BECN1 and LC3 and also the apoptotic index were up regulated in testicular cultures subjected to nutritional stress. These results suggest a possible interaction between apoptosis and autophagy in the active and activating testis (characterized by high metabolic requirement and nutrient), where autophagy could promote survival over cell death. In the inactive testis, the absence of autophagic-related proteins might explain the massive loss of germ cells, suggesting that autophagy plays new and key role in the alterations of the seminiferous epithelium during photoregression.
Abstract. Androgens and androgen receptor play a critical role in spermatogenesis and fertility in mammals, and estrogens and their receptors contribute to regulation of testicular function through initiation and maintenance of spermatogenesis and germ cell division and survival. However, results from different species are still far from establishing a clear understanding of these receptors in the different cell types from the testis. We analyzed the expression of androgen receptor, estrogen receptors α and β and aromatase protein by immunohistochemistry and real-time PCR, in relation to proliferation followed by the expression of proliferation cell nuclear antigen (PCNA) and germinal identity by VASA protein, in fetal, perinatal, prepubertal and adult testes of Lagostomus maximus, a rodent with sustained germ cell proliferation and an increasing number of OCT-4-expressing gonocytes in the developing ovary. AR expression was restricted to Leydig cells and peritubular cells before sexual maturity, at which point it also became expressed in Sertoli cells. ERα and ERβ were expressed in seminiferous tubules and the interstitium, respectively, in both fetal and prepubertal testes. In adult testes, both ERα and ERβ co-localized in Leydig and peritubular cells. The aromatase enzyme, which converts androgenic precursors into estrogens, was detectable in all developmental stages analyzed and was restricted to Leydig cells. PCNA remained high until sexual maturity. A ndrogens and the androgen receptor (AR) have been shown to play a critical role in normal spermatogenesis and fertility in mammals [1]. The testosterone, responsible for inducing meiosis, postmeiotic development and inhibiting apoptosis in the germ cell, is produced in the testis by the Leydig cells and binds to the AR modulating gene transcription in Leydig, Sertoli, peritubular and germ cells [2]. It has been clearly established that the AR is expressed in Sertoli, Leydig and peritubular cells in the mammalian testis. However, immunodetection of the AR in testicular germ cells is controversial, with reports indicating its detection and absence, although functional AR in germ cells is not essential for spermatogenesis and male fertility in mice [3].Estrogens have been shown to largely contribute to the regulation of testicular function [4,5], acting on the initiation and maintenance of spermatogenesis and on germinal stem cell division and survival [5]. Estrogen action is displayed by means of two different estrogen receptors (ERs), estrogen receptor-alpha (ERα) and estrogen receptor-beta (ERβ), localized in the different testicular cells types. The localization of ERs in testicular cells is not only species-specific but it also varies depending on the type of receptor and the developmental stage of the germ cell [6][7][8][9][10]. In most species analyzed (e.g., human, rat, cat, dog), ERα and ERβ co-localize in spermatogonia, spermatocytes and spermatids as well as in Sertoli, Leydig, and peritubular cells [9,10]. In other species, such as the boar, ERα and ...
Cell proliferation and cell death are essential processes in the physiology of the developing testis that strongly influence the normal adult spermatogenesis. We analysed in this study the morphometry, the expression of the proliferation cell nuclear antigen (PCNA), cell pluripotency marker OCT-4, germ cell marker VASA and apoptosis in the developing testes of Lagostomus maximus, a rodent in which female germ line develops through abolished apoptosis and unrestricted proliferation. Morphometry revealed an increment in the size of the seminiferous cords with increasing developmental age, arising from a significant increase of PCNA-positive germ cells and a stable proportion of PCNA-positive Sertoli cells. VASA showed a widespread cytoplasmic distribution in a great proportion of proliferating gonocytes that increased significantly at late development. In the somatic compartment, Leydig cells increased at mid-development, whereas peritubular cells showed a stable rate of proliferation. In contrast to other mammals, OCT-4 positive gonocytes increased throughout development reaching 90% of germ cells in late-developing testis, associated with a conspicuous increase in circulating FSH from mid- to late-gestation. TUNEL analysis was remarkable negative, and only a few positive cells were detected in the somatic compartment. These results show that the South American plains viscacha displays a distinctive pattern of testis development characterized by a sustained proliferation of germ cells throughout development, with no signs of apoptosis cell demise, in a peculiar endocrine in utero ambiance that seems to promote the increase of spermatogonial number as a primary direct effect of FSH.
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