Dynamic changes in mitochondrial 3D structure during folliculogenesis and luteal formation in the goat large luteal cell lineage

Yi-Fan Jiang,Yovita Permata Budi,Chih-Hsien Chiu,Pin-Huan Yu,Chi-Yu Fu

doi:10.1038/s41598-021-95161-w

Yi-Fan Jiang, Yovita Permata Budi + Show 3 more

Open Access

https://doi.org/10.1038/s41598-021-95161-w

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Abstract

In mammalian ovaries, mitochondria are integral sites of energy production and steroidogenesis. While shifts in cellular activities and steroidogenesis are well characterized during the differentiation of large luteal cells in folliculogenesis and luteal formation, mitochondrial dynamics during this process have not been previously evaluated. In this study, we collected ovaries containing primordial follicles, mature follicles, corpus hemorrhagicum, or corpus luteum from goats at specific times in the estrous cycle. Enzyme histochemistry, ultrastructural observations, and 3D structural analysis of serial sections of mitochondria revealed that branched mitochondrial networks were predominant in follicles, while spherical and tubular mitochondria were typical in large luteal cells. Furthermore, the average mitochondrial diameter and volume increased from folliculogenesis to luteal formation. In primordial follicles, the signals of cytochrome c oxidase and ATP synthase were undetectable in most cells, and the large luteal cells from the corpus hemorrhagicum also showed low enzyme signals and content when compared with granulosa cells in mature follicles or large luteal cells from the corpus luteum. Our findings suggest that the mitochondrial enlargement could be an event during folliculogenesis and luteal formation, while the modulation of mitochondrial morphology and respiratory enzyme expressions may be related to tissue remodeling during luteal formation.

Highlights

Mitochondria are structurally unique organelles that serve as the power plant of the cell and as a signaling platform in cell physiology
Since the content and quality of mitochondria can be regulated by mitochondrial dynamics, biogenesis and mitophagy, the morphology of mitochondrial networks may reflect various roles played by the organelle at specific stages of cell d ifferentiation[6]
Mitochondria are involved in apoptosis, ATP production and steroidogenesis at various stages of differentiation in the LLC linage

Summary

Introduction

Mitochondria are structurally unique organelles that serve as the power plant of the cell and as a signaling platform in cell physiology. Mitochondria are organelles with double membranes called the outer mitochondrial membrane (OMM) and the inner mitochondrial membrane (IMM). Mitochondrial ATP production requires the consumption of intracellular oxygen to support cellular functions and cell survival, but a toxic byproduct of mitochondrial oxygen consumption is the generation of reactive oxygen species (ROS). Imbalances in mitochondrial ATP and ROS production may lead to cell death via opening of the mitochondrial permeability transition pore on the surface of mitochondria and subsequent activation of a poptosis[3]. Besides their role in energy production, mitochondria in cells of the LLC lineage provide a regulatory site for steroidogenesis; the rate-limiting steps of P 4 production are mitochondrial cholesterol transport and a side-chain cleavage reaction by the mitochondrial enzyme CYP11A15. To examine fine structural details, 3D reconstructions of cellular structures and enzyme activities were made at an ultrastructural level

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