The Organization of the Golgi Structures during Drosophila Male Meiosis Requires the Citrate Lyase ATPCL

Morciano, Patrizia; Giorgio, Maria Laura Di; Tullo, Liliana; Cenci, Giovanni

doi:10.3390/ijms22115745

Cited by 2 publications

References 24 publications

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Metabolic regulation of proteome stability via N-terminal acetylation controls male germline stem cell differentiation and reproduction

François,

Pihl,

Dunoyer de Segonzac

et al. 2023

Nat Commun

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The molecular mechanisms connecting cellular metabolism with differentiation remain poorly understood. Here, we find that metabolic signals contribute to stem cell differentiation and germline homeostasis during Drosophila melanogaster spermatogenesis. We discovered that external citrate, originating outside the gonad, fuels the production of Acetyl-coenzyme A by germline ATP-citrate lyase (dACLY). We show that this pathway is essential during the final spermatogenic stages, where a high Acetyl-coenzyme A level promotes NatB-dependent N-terminal protein acetylation. Using genetic and biochemical experiments, we establish that N-terminal acetylation shields key target proteins, essential for spermatid differentiation, from proteasomal degradation by the ubiquitin ligase dUBR1. Our work uncovers crosstalk between metabolism and proteome stability that is mediated via protein post-translational modification. We propose that this system coordinates the metabolic state of the organism with gamete production. More broadly, modulation of proteome turnover by circulating metabolites may be a conserved regulatory mechanism to control cell functions.

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Metabolic regulation of proteome stability via N-terminal acetylation controls male germline stem cell differentiation and reproduction

François,

Pihl,

Dunoyer de Segonzac

et al. 2023

Nat Commun

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Glucose-6-phosphatase is required for organelle reorganization, energy metabolism and motility ofDrosophilasperm

Hedjazi,

Miyamoto,

Ahn

et al. 2024

Preprint

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Glucose-6-Phosphatase (G6Pase), a key enzyme in gluconeogenesis and glycogenolysis in the mammalian liver and kidney, converts glucose-6-phosphate to glucose to maintain systemic blood glucose homeostasis during nutrient deprivation. However, its function has remained elusive in insects which have no need for G6Pase in sugar homeostasis, since they use trehalose as the main circulating sugar and convert glucose-6-phosphate to trehalose via trehalose phosphate synthase (TPS1). This study reveals an unexpected and essential role for G6Pase in Drosophila fertility. We report that that Drosophila G6P mutant males are sterile and show that G6Pase plays an essential role to produce motile sperm. While spermatogenesis and spermiogenesis in G6P mutant males appears to proceed normally, leading to the production and transfer of mature sperm, G6P- sperm tail beat frequency is severely diminished in the female reproductive tract, and sperm only rarely enter an egg. Moreover, when compared to wild type sperm, G6P- sperm are depleted earlier from spermathecae and seminal receptacle. Immunohistochemical analyses show that G6P mutant spermatocytes present with an enlarged and stressed endoplasmic reticulum (ER) and a diminished Golgi. Additionally, the acrosome, a Golgi derived organelle critical for sperm-egg interaction, is partially depleted of the transmembrane protein SNEAKY, which is essential to breakdown the sperm plasma membrane after fertilization. Metabolic analyses show that both basal and compensatory glycolysis and ATP production are compromised in testes of G6P mutant males. Based on these observations, we propose a model in which Drosophila G6Pase functions as a metabolite repair enzyme in spermatocytes. By removing a non-canonical metabolite, G6Pase facilitates glycolysis to meet the high energy demands of spermatogenesis and sperm cell differentiation. Thus, our investigations unveil a novel function for G6Pase in male fertility, highlighting its importance in regulating energy homeostasis in reproductive tissues.

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The Organization of the Golgi Structures during Drosophila Male Meiosis Requires the Citrate Lyase ATPCL

Cited by 2 publications

References 24 publications

Metabolic regulation of proteome stability via N-terminal acetylation controls male germline stem cell differentiation and reproduction

Metabolic regulation of proteome stability via N-terminal acetylation controls male germline stem cell differentiation and reproduction

Glucose-6-phosphatase is required for organelle reorganization, energy metabolism and motility ofDrosophilasperm

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