The Bidder's organ of the toad Rhinella arenarum (Amphibia, Anura). Presence of steroidogenic enzymes

Abstract

The Bidder's organ (BO) of male true toads of Bufonidae family is located in the anterior pole of the testis and it has been compared to a rudimentary ovary because of the presence of previtellogenic follicles. In some species, BO remains in both sexes, while in others only adult males preserve the structure. Several studies suggest that the development of BO is inhibited by the differentiation of the corresponding gonad. The purpose of this study is to describe morphological and histological variability of the BO of Rhinella arenarum and also analyze its steroidogenic capacity. Observations indicate that although most bidderian follicles are in pre vitellogenesis, there are others in early or late vitellogenesis. Moreover, we found that BOs weight was significantly lower in males during the pre-reproductive period and that there is no significant correlation between the weights of BO and the adjacent testis. We also analyzed the presence of steroidogenic enzymes using immunohistochemistry. Results indicate that all the follicles were immunoreactive with the antibody against aromatase, while only few of them were positive for the cytochrome P450 side-chain cleavage. Furthermore, activities of 3β-hydroxysteroid dehydrogenase/isomerase, cytochrome P450 17-hydroxylase, C17,20-lyase and aromatase were detected by the transformation of radioactive substrates into products. Taken together, these results confirm the steroidogenic capacity of the BO in adult males of R. arenarum.

Bidder’s organ – structure, development and function

“…This variability has also been shown to be associated with environmental pollutants and seasonal activity (Scaia et al, 2008(Scaia et al, , 2011. There are also examples of individuals with well-developed Bidder's organs and small remnants of testes (Bufo woodhousii;Pancak, 1987).…”

“…Despite the fact that the presence of Bidder's organ has been described in many bufonid species, and that the removal of testes leads to transformation of Bidder's organs into ovaries, which indicates that Bidder's organs represent developmentally inhibited ovaries, the role of these organs is still unclear (Table 1; Harms, 1923;Ponse, 1924;Tanimura and Iwasawa, 1986;Duellman and Trueb, 1994;Abramyan et al, 2010. Although commonly accepted belief is that Bidder's organs are rudimentary or vestigial structures, some investigators believe that they are fully functional steroidogenic organs important for reproduction control (Davies, 1936;Colombo and Colombo-Belvedere, 1980;Abramyan et al, 2010;Scaia et al, 2011).…”

“…There is a discrepancy in the literature concerning the presence of vitellogenic oocytes in Bidder's organs. The majority of studies have shown that the vitellogenic oocytes appear in Bidder's organ only after orchidectomy (testis removal) ( Table 1; Ponse, 1927;Pancak-Roessler and Norris, 1991), however, some authors described the presence of vitellogenic oocytes in Bidder's organs of Bufo marinus or Bufo arenarum during a reproductive season when these organs grow (McCoy et al, 2008;Scaia et al, 2011). Moreover, the lampbrush chromosomes, characteristic of intensively RNA-synthesizing anuran oocytes, were described in the oocytes of Bidder's organs in B. marinus, Bufo terrestris, Bufo woodhousii, which indicates high metabolic activity of bidderian oocytes (Eichler, 1976).…”

“…The enzymes responsible for synthesis of androgens and estrogens (3bHSD, 17bHSD) from cholesterol are present in the ooplasm of bidderian oocytes and in the follicular cells in B. arenarum, B. melanostictus and B. woodhousii (Ghosh, 1982;Pancak-Roessler and Norris, 1991;Scaia et al, 2011). Bidder's organ is capable of converting pregnenolone or progesterone into several steroid hormones such as 17-hydroxyprogesterone, androstendione, testosterone, 17b-estradiol and estrone (Colombo and Colombo-Belvedere, 1980).…”

“…Bidder's organ is capable of converting pregnenolone or progesterone into several steroid hormones such as 17-hydroxyprogesterone, androstendione, testosterone, 17b-estradiol and estrone (Colombo and Colombo-Belvedere, 1980). In B. arenarum the enzyme converting cholesterol into pregnenolone was detected in follicular cells only in few follicles, however, aromatase was present in all bidderian follicles (Scaia et al, 2011). In bufonids B. marinus, B. bufo, B. arenarum testes do not produce estradiol, however, the estradiol synthesis was detected in their Bidder's organs (Kime and Hews, 1978;Colombo and Colombo Belvedere, 1980;Canosa et al, 1998).…”