Regulation of meiotic telomere dynamics through membrane fluidity promoted by AdipoR2-ELOVL2

Jingjing Zhang, Mario Ruiz, Per-Olof Bergh, Marcus Henricsson, Nena Stojanović, Ranjan Devkota, Marius Henn, Mohammad Bohlooly-Y, Abrahan Hernández-Hernández, Manfred Alsheimer, Jan Borén, Marc Pilon () and Hiroki Shibuya ()
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Jingjing Zhang: University of Gothenburg
Mario Ruiz: University of Gothenburg
Per-Olof Bergh: University of Gothenburg
Marcus Henricsson: University of Gothenburg
Nena Stojanović: University of Gothenburg
Ranjan Devkota: University of Gothenburg
Marius Henn: University of Würzburg
Mohammad Bohlooly-Y: BioPharmaceuticals R&D, AstraZeneca
Abrahan Hernández-Hernández: Karolinska Institutet
Manfred Alsheimer: University of Würzburg
Jan Borén: University of Gothenburg
Marc Pilon: University of Gothenburg
Hiroki Shibuya: University of Gothenburg

Nature Communications, 2024, vol. 15, issue 1, 1-14

Abstract: Abstract The cellular membrane in male meiotic germ cells contains a unique class of phospholipids and sphingolipids that is required for male reproduction. Here, we show that a conserved membrane fluidity sensor, AdipoR2, regulates the meiosis-specific lipidome in mouse testes by promoting the synthesis of sphingolipids containing very-long-chain polyunsaturated fatty acids (VLC-PUFAs). AdipoR2 upregulates the expression of a fatty acid elongase, ELOVL2, both transcriptionally and post-transcriptionally, to synthesize VLC-PUFA. The depletion of VLC-PUFAs and subsequent accumulation of palmitic acid in AdipoR2 knockout testes stiffens the cellular membrane and causes the invagination of the nuclear envelope. This condition impairs the nuclear peripheral distribution of meiotic telomeres, leading to errors in homologous synapsis and recombination. Further, the stiffened membrane impairs the formation of intercellular bridges and the germ cell syncytium, which disrupts the orderly arrangement of cell types within the seminiferous tubules. According to our findings we propose a framework in which the highly-fluid membrane microenvironment shaped by AdipoR2-ELOVL2 underpins meiosis-specific chromosome dynamics in testes.

Date: 2024
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DOI: 10.1038/s41467-024-46718-6

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