Involution processes of follicular atresia and post-ovulatory complex in a characid fish ovary: a study of apoptosis and autophagy pathways

Abstract

Recent studies seem to indicate that apoptosis and autophagy can act cooperatively in fish ovaries in order to achieve more effective ovarian regression after spawning. Considering the importance of tissue remodeling in ovarian functioning, we sought to morphologically characterize the involution processes of follicular atresia and post-ovulatory complexes using Astyanax altiparanae as an experimental model, and to determine the location of proteins involved in apoptosis and autophagy throughout this process. Fifteen females were collected after reproductive management. Fragments of the left ovaries were removed, fixed, and prepared for light microscopy and immunofluorescence analyses. The main characteristics of the involution processes were found to be consistent with previous descriptions. However, there were certain morphological peculiarities that do not appear to have been described for any other species thus far. These peculiarities may be related to the focus of this study on a single species, which allows for a more detailed investigation into morphological changes than studies on multiple species. Autophagy was also found to precede apoptosis in both involution processes in A. altiparanae. This may be related to the energy recycling process required before the removal of degenerated follicular cells by apoptosis. Thus, these results support the idea that there is crosstalk between autophagy and apoptosis pathways in ovarian involution processes, as well as the idea that the cell death pathways of these processes are conserved between teleost species with external fertilization.

Autophagy and Cathepsin D mediated apoptosis contributing to ovarian follicular atresia in the Nile tilapia

“…However, nonapoptotic processes, such as autophagy, can contribute to the efficient elimination of granulosa cells in mammals (Repnik Meng et al, 2018). In teleost fish, recent studies indicate that autophagy can be involved in follicular atresia (Cassel, Camargo, Jesus, & Borella, 2017;Morais, Thomé, Lemos, Bazzoli, & Rizzo, 2012;Morais, Thomé, Santos, Bazzoli, & Rizzo, 2016;Thomé et al, 2009), but the interactions between these signaling pathways are not fully elucidated.…”

Morphological patterns of cell death in ovarian follicles of primary and secondary growth and postovulatory follicle complex of the annual killifish Millerichthys robustus (Cyprinodontiformes: Cynolebiidae)

“…Interestingly, in this investigation, the postovulatory morphology of the POF follicular cells became columnar again, revealing secretory activity (Drummond et al, ). This morphological change was also described in the POC's of Prochilodus costatus , at 24 hr postovulation (Gruppi et al, ), Astyanax bimaculatus (Drummond et al, ), and A. altiparanae (Cassel et al, ).…”

“…In this research, follicular atresia had a higher prevalence in follicles of secondary growth stage than in earlier stages, because large follicles contain considerable more amount of available energy than follicles in previous stages (Cassel, Camargo, Wender, & Borella, ; Quirk, Cowan, Harman, Hu, & Porter, ; Wood & Van Der Kraak, ), allowing to recycle both the energy and constitutive elements of the oocyte invested during their development (Blazer, ; Miranda et al, ; Wood & Van der Kraak, ). Moreover, the incidence of atresia in follicles of the primary growth stage may involve the selection and recruitment of groups of follicles able to perform vitellogenesis and subsequent stages of development (Drummond, Bazzoli, Rizzo, & Sato, ; Janz & Van der Kraak, ).…”

“…Despite this, low or none hormonal activity of POC has been documented (Selman & Wallace, ), thus equivalence with the corpus luteum of mammals is highly unlikely due to the short duration in fishes (Grier et al, ; Lang, ). Cassel et al () related the vesicles inside the follicular cells of POF and their columnar morphology with activity of synthesis of glycoproteins, probably associated with secretion, self‐digestion, or both. In this context, Smith and Haley (, ) revealed steroidogenic activity (estradiol and testosterone) in follicular cells and theca in POC of Oreochromis mossambicus , suggesting the possibility that the secretion of these steroids is related to the development of surrounding follicles and proliferation of oogonia (Grier et al, ).…”

A Review of the Macroscopic, Microscopic, and Ultramicroscopic Characteristics of Some Key Oocyte Developmental Processes in Fish Species

“…The morphological characteristics of the atretic bodies and their stages of involution, independent of cellular development stage, were summarized in the study of Miranda et al [20], as (1) initial atresia, with the disintegration of the oocyte nucleus, fragmentation of the zona pellucida, and follicular cell hypertrophy; (2) intermediate atresia, with follicular cells presenting phagocytic characteristics and ingesting the yolk; (3) advanced atresia, with numerous myelinic figures in the cytoplasm of follicular cells; and (4) final atresia, with the reduction in the number of follicular and theca cells and presence of granules of lipofuscin and granulocytes near the atretic follicle. With the current emergence of the theme of cell death pathways, studies about ovarian involutive processes in fish were brought to the spotlight again with new descriptions being made [102,108,116,[119][120][121][122][123][124]] that add and/or corroborate those morphological characteristics already proposed by Miranda et al [20].…”