Naturally suppressed apoptosis prevents follicular atresia and oocyte reserve decline in the adult ovary of Lagostomus maximus (Rodentia, Caviomorpha)

• Published in: Reproduction (Cambridge, England) Vol. 132; no. 2; pp. 301 - 308
• Main Authors: Jensen, Federico, Willis, Miguel A, Albamonte, Mirta S, Espinosa, María B, Vitullo, Alfredo D
• Format: Journal Article
• Language: English
• Published: Colchester Society for Reproduction and Fertility 01.08.2006; BioScientifica Ltd; Portland
• Subjects: animal proteins; Animals; Apoptosis; Apoptosis Regulatory Proteins - analysis; Apoptosis Regulatory Proteins - physiology; bcl-2-Associated X Protein - analysis; Biological and medical sciences; Blotting, Western - methods; Caviidae; DNA fragmentation; Estrogen Receptor alpha - analysis; estrogens; Female; Follicular Atresia; follicular development; Follicular Phase; Fundamental and applied biological sciences. Psychology; gene expression; hormone receptors; immunohistochemistry; Immunohistochemistry - methods; In Situ Nick-End Labeling; Mammalian female genital system; Morphology. Physiology; multigene family; oocytes; Oocytes - cytology; Ovarian Follicle - chemistry; ovarian follicles; ovaries; ovulation; polyovulation; Pregnancy; progesterone; Proto-Oncogene Proteins c-bcl-2 - analysis; Receptors, Progesterone - analysis; Rodentia - physiology; South America; Vertebrates: reproduction; wild animals; South America; Ovary; Vertebrata; Reproduction; Mammalia; Cell death; Female genital system; Rodentia; Atresia; Germinal cell; Oocyte; Apoptosis
• ISSN: 1470-1626; 1741-7899
• DOI: 10.1530/rep.1.01054

It has been widely accepted that mammalian females are born with a non-renewing, finite pool of oocytes that will be continuously cleared by atresia, with only a small proportion of them reaching ovulation. Apoptosis regulates this mass germ cell death, especially through the balance between pro- and anti-apoptotic proteins encoded by the BCL-2 gene family. The caviomorph rodent Lagostomus maximus, the South American plains viscacha, displays the highest ovulation rate known for a mammal releasing 400–800 eggs per cycle. We tested the hypothesis that in L. maximus massive polyovulation is a consequence of reduced apoptosis resulting in suppressed follicular atresia. We found that anti-apoptotic BCL-2 gene is markedly expressed in all kind of follicles from primordial to fully mature antral stages in the adult ovary of L. maximus. On the other hand, pro-apoptotic BAX gene showed weak signals or was undetectable by immunohistochemical examination. Western blot against both proteins confirmed immunohistochemical results. Screening for DNA fragmentation by TUNEL assay was conspicuously negative in ovaries from both pregnant and non-pregnant females. In addition, α-oestrogen receptor also showed an enhanced expression from primordial stage to fully mature antral follicles. Our results show that natural preferential expression of BCL-2 and restricted BAX expression greatly suppresses apoptosis in the ovary of L. maximus. This prevents the decline of the oocyte reserve by abolishing follicular atresia and enables the highest ovulation rate known for a mammal, 400–800 or more eggs per cycle.