The Mussel Mytilus galloprovincialis in the Bay of Naples: New Insights on Oogenic Cycle and Its Hormonal Control

Abstract

The aim of the present article was to investigate the oogenic cycle of Mytilus galloprovincialis sampled in the Bay of Naples, and to immunolocalize 3β‐hydroxysteroid dehydrogenase (3β‐HSD), 17β‐hydroxysteroid dehydrogenase (17β‐HSD), and P450 aromatase, enzymes involved in the synthesis of two sex hormones: testosterone and 17β‐estradiol. We demonstrate that the oogenic cycle starts in late summer‐early fall and continues in early winter when the first event of spawning occurs; other spawning events take place until June, when the ovary is spent and contains a few empty ovarian follicles and numerous somatic cells, that is, adipogranular cells and vesicular connective tissue cells. During the oogenic cycle, apoptotic events occur at the level of oogonia, previtellogenic oocytes, as well as follicle cells; by contrast, necrosis events probably take place in vitellogenic oocytes, which, once degenerated, transfer their content to healthy oocytes. Finally, the present data demonstrate that 3β‐HSD, 17β‐HSD, and P450 aromatase are present in the ovary both during the reproductive and nonreproductive phases. The possible role of these enzymes during the Mytilus galloprovincialis reproductive cycle is discussed. Anat Rec, 302:1039–1049, 2019. © 2019 Wiley Periodicals, Inc.

Seasonal expression and cellular distribution of star and steroidogenic enzymes in quail testis

“…In the testis, they are primarily produced in Leydig and Sertoli cells, where they are synthesized from a common precursor, the cholesterol, via a series of enzyme‐catalyzed reactions (Miller, ). However, in recent years it has been showed that germ cells also produce sex hormones (Agnese et al, ; Carreau et al, ; Prisco et al, ; Rosati, Agnese, et al, ; Rosati, Agnese, Abbagnale, et al, ; Rosati, Santillo, et al, ). Indeed, more recently, in some seasonal breeding, as the bivalve mollusk Mytilus galloprovincialis and the squamous reptile Podarcis sicula, we highlighted that not only the somatic cells, but also the germ cells are involved in the steroidogenesis synthesis.…”

The expression of estrogen receptors during the Mytilus galloprovincialis ovarian cycle

“…It is to be noted that the ER1 and ER2 expression within the growing oocytes, follicular, and adipogranular cells overlaps with the expression of the mRNA for vitellogenin, strongly suggesting that in Mytilus , as in vertebrates studied so far, the expression of vitellogenin is under the control of estrogens and is mediated by receptors. It is worth to note that the same cells are equipped with the key enzyme that control the sex hormone synthesis (Rosati, Agnese, et al, ; Rosati, Prisco, et al, ). Considering that ER1 is up and downstream factors activated by downstream factors via feedback mechanisms (Horard & Vanacker, ; Nagasawa et al, ), whereas ER2 is responsive to estrogens, it is quite probably that in M. galloprovincialis ER1 and ER2, differently attend in the gametogenesis: ER1 mainly in the spawning and ER2 in the oocyte growth, particularly in vitellogenesis.…”

“…Twenty‐five females for each phase of the reproductive cycle (Stages 0–III; Dunker et al, 2008) were used. Specimens were collected in the Bay of Naples as previously reported for the males (Prisco, Agnese, De Marino, Andreuccetti, & Rosati, ; Rosati, Prisco, et al, ). The ovaries, excised using sterile RNase‐free dissecting equipment, were either frozen on dry ice and stored at −80°C or fixed for 24 hr in Bouin's solution, dehydrated with graded ethanol and embedded in paraffin wax.…”

“…Moreover, in M. edulis and Mytilus galloprovincialis , it has been identified a typical receptor of estrogen, reported also as ER2, as well as an estrogen‐related receptor not activated by estrogens, reported also as ER1 (Nagasawa et al, ). More recently, in M. galloprovincialis we highlighted a different expression of ER mRNA collected in different areas of Naples bay (Rosati, Agnese, et al, ), and the presence of key steroid sex hormone biosynthesis enzymes in the same cells (Rosati, Prisco, et al, ) engaged into the vitellogenesis (Agnese, Prisco, et al, ; Agnese, Verderame, et al, ).…”

“…The aim of this study is to identify, by real‐time polymerase chain reaction (RT‐PCR) and in situ hybridization, the ER expression in the ovary of M. galloprovincialis collected in the Naples Bay, during the different phases of the cycle, that is Stage 0 (stasis and previtellogenesis), Stage I (beginning of the oocyte growth), Stage II (vitellogenesis), and Stage III, the final stage of the oocyte growth, when the ovary is ripe and the full‐grown oocytes have to be stanned, as previously reported (Agnese, Prisco, et al, ; Agnese, Verderame, et al, ; Duinker, Haland, Hovgaard, & Mortensen, ; Rosati, Agnese, et al, ; Rosati, Prisco, et al, ).…”