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The ultra-structures, components, and functions of intermitochondrial cement (IMC) and mitochondria-associated ER membranes (MAMs) in male germ cells are summarized. We also discuss the roles of the structural components in piRNA biogenesis and propose that further study could unravel new insights into mitochondria-associated germinal structures in spermatogenesis. We summarize the ultra-structure of IMC and MAMs in mouse spermatocyte, as shown in Figure 1A. In this review, we review the insights gained from studying the structural components of mitochondria-associated germinal structures, including IMC, CB, and MAMs, which are pivotal structures to ensure genome integrity and male fertility. However, the functions of MAMs are still mysterious in spermatogenesis. Our previous work reported that MAMs are abundant in both human and mouse spermatogenic cells, and contain many crucial proteins that are associated with the Piwi-interacting RNA (piRNA) pathway. Disturbances to MAMs lead to neurodegenerative diseases and cancer. MAMs participate in several cellular signaling pathways, including calcium transmission, phospholipid exchange, intracellular trafficking, autophagy, ER stress, mitochondrial biogenesis, and inflammasome formation. Mitochondria-associated ER membranes (MAMs) are tight structural contacts, also named as MERCs (mitochondria-ER contacts) ~20% of the mitochondrial surface are jointly opposing and contact directly with the ER, yielding to approximately 10 and 30 nm in distance. Nuage are characterized by an amorphous shape, the absence of surrounding membranes, an abundance of RNAs and proteins, and a close association with mitochondria clusters or immediately adjacent to the nuclear envelope of germ cells, including intermitochondrial cement (IMC, also named pi-body), piP-body, and chromatoid body (CB) in mammalian germ cells, according to their localization, morphology, and/or biochemical properties. Over 80 animals in eight phyla are reported as having a nuage structure in their germ cells. Since the advent of electron microscopy, particular attention has been paid to the unique structure in germ cells, termed as nuage, the French word for cloud, initially employed by Andri and Rouiller in 1957.
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We discuss the roles of the structural components in spermatogenesis and piRNA biogenesis, which provide new insights into mitochondria-associated germinal structures in germ cell development and male reproduction. Here, we review the insights gained from studying the structural components of mitochondria-associated germinal structures, including IMC, CB, and MAMs, which are pivotal structures to ensure genome integrity and male fertility. Although little is known about the formation of both IMC and MAMs, its distinctive characters have attracted considerable attention. Provocatively, IMC functionally communicates with other nuage structures, such as piP-body, to perform its complex functions in spermatogenesis. Importantly, our previous work reported that mitochondria-associated ER membranes (MAMs) are abundant in spermatogenic cells and contain many crucial proteins associated with the piRNA pathway. IMC is primarily enriched with various Piwi-interacting RNA (piRNA) proteins and mainly functions as piRNA biogenesis, transposon silencing, mRNA translation, and mitochondria fusion. The most relevant nuage structure with mitochondria is IMC, also called pi-body, present in prospermatogonia, spermatogonia, and spermatocytes. Since mitochondria exhibit different morphology and topographical arrangements to accommodate specific needs during spermatogenesis, the distribution of mitochondria-associated nuage is also dynamic. Multiple specific granular structures are present in the cytoplasm of germ cells, termed nuage, which are electron-dense, non-membranous, close to mitochondria and/or nuclei, variant size yielding to different compartments harboring different components, including intermitochondrial cement (IMC), piP-body, and chromatoid body (CB).