Proliferation and apoptosis in the seminiferous epithelium of photoinhibited Syrian hamsters (Mesocricetus auratus)¹

Abstract

In the hamster, male reproductive quiescence is accomplished via testicular atrophy and the germinal epithelium is regressed to spermatogonia and spermatocytes after 8-14 weeks of short photoperiods. However, the cellular mechanisms involved in this process have not been elucidated. As it is suggested that the regulation of seasonal testicular activity is characterized by coordinated shifts in the relationships between mitosis, meiosis and apoptosis, the changes in the proliferative and apoptotic activity in the seminiferous epithelium of photoinhibited Syrian hamster were examined and compared with those maintained in natural photoperiod. The proliferative activity was studied using BrdU immunostaining, and germ cell apoptosis was assessed by in situ TUNEL labelling and transmission electron microscopy. A significant increase in the rate of apoptosis (percentage of TUNEL-positive spermatogonia + spermatocytes) was observed in photoinhibited animals (2.84 +/- 0.16) compared with those exposed to natural photoperiod (0.77 +/- 0.03, p < 0.05). The majority of apoptotic germ cells were spermatocytes and in some occasions spermatogonia. Germ cell apoptosis was confirmed by morphological characteristics: condensation of the chromatin and nuclear fragmentation. The rate of proliferation (percentage of BrdU-positive spermatogonia + preleptotene spermatocytes) was significantly higher in photoinhibited hamsters (42.7 +/- 2.6) compared with animals exposed to natural photoperiod (31.1 +/- 1.6, p < 0.05). After the exposure to a short photoperiod the apoptotic index positively correlated with the proliferative index (r = 0.8150, p < 0.05). In conclusion, the seminiferous epithelium of photoinhibited Syrian hamsters is characterized by an increased rate of apoptosis associated to an enhanced rate of proliferation.

Apoptosis, proliferation, and cell size in seasonal changes of body and organ weight in male bank voles Myodes glareolus

“…The results of the present study confirmed previous observations that changes in the number of testicular cells are responsible for the seasonal changes of testes weight in small mammals sensitive to photoperiod (Young et al 1999;Young and Nelson 2001;Morales et al 2002;Sato et al 2005;Pastor et al 2011;Seco-Rovira et al 2014). In contrast to the testes, changes in the number of myocytes and hepatocytes appeared not to significantly contribute to the seasonal changes of body (muscle) and liver weights in the bank vole.…”

“…Apoptosis allows to eliminate excessive or unnecessary cells without negative consequences for the remaining cells, and it is involved in the control of cell differentiation and remodeling of embryonic tissues (Fuchs and Steller 2011), the involution of some organs such as the mammary gland and thymus (Hojilla et al 2011;Linkova et al 2011), and aging (Zhang et al 2003). Moreover, previous studies on mammals sensitive to changes in daylength showed that apoptosis is responsible for testicular regression (Young et al 1999;Young and Nelson 2001;Morales et al 2002;Strbenc et al 2003;Luaces et al 2014). However, it is unknown whether this process is involved in the regression of other organs and tissues such as the liver and skeletal muscles.…”

Testicular histomorphometry and the proliferative and apoptotic activities of the seminiferous epithelium in Syrian hamster (Mesocricetus auratus) during regression owing to short photoperiod

“…In contrast, in the Syrian hamster there is some controversy about whether there is a higher or lower spermatogonia PI in fully regressed testes. These differences may be because of the method used to calculate this index because the lowest PI was observed by studying the mitotic activity (do Nascimento et al, 2009), whereas the highest proliferative index was observed by studying cells entering proliferation (Morales et al, 2002). In addition, do Nascimento's calculation was performed considering the number of Sertoli cells to be constant, whereas they decrease in numbers during regression (Seco-Rovira et al, 2014) so the index would be biased.…”

“…In contrast, in the white-footed mouse, starling (Young & Nelson, 2001) or the crow (Jenkins et al, 2007;Islam et al, 2012) it has been observed that, in addition to apoptosis in spermatocytes, apoptosis also occurs in round spermatids and spermatogonia, although to a lesser extent, while spermatogenesis arrest, occurs in spermatogonia. To date, the Syrian hamster has been classified as a species where apoptosis is important but not the main mechanism of testicular regression, owing to the lack of data concerning the changes that occur during testicular regression (Dadhich et al, 2013), although it is known that spermatocyte apoptosis is crucial for maintaining regression once it is already established (Morales et al, 2002). In this study, the effect of short photoperiod has been studied throughout the whole process of testicular regression, so that it is possible to conclude that apoptosis plays an essential role in the atrophy of the seminiferous epithelium during the non-breeding season.…”

Circannual Testis Changes in Seasonally Breeding Mammals

“…In both species, the inactive testis maintains some meiotic activity, as meiosis onset is not completely interrupted and some few primary spermatocytes are still present in the regressed seminiferous tubules [Dadhich et al, 2010[Dadhich et al, , 2013. This situation appears to be quite common in many species that undergo seasonal testis regression, as observed in the Japanese redbellied newt, Cynops pyrrhogaster [Yazawa et al, 2000], the silver fox, Vulpes vulpes [Andersen Berg et al, 2001], the Syrian hamster [Morales et al, 2002[Morales et al, , 2007, the Chinese soft-shelled turtle, Pelodiscus sinensis [Zhang et al, 2008], and the Japanese jungle crow, Corvus macrorhynchos [Islam et al, 2012], as well as in the Mediterranean pine vole, Microtus duodecimcostatus [unpubl. data], among others.…”