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[Preprint]. 2023 Oct 31:2023.07.31.551250. [Version 3] doi: 10.1101/2023.07.31.551250

Epi-microRNA mediated metabolic reprogramming ensures affinity maturation

Rinako Nakagawa, Miriam Llorian, Sunita Varsani-brown, Probir Chakravarty, Jeannie M Camarillo, David Barry, Roger George, Neil P Blackledge, Graham Duddy, Neil L Kelleher, Rob J Klose, Martin Turner, Dinis Pedro Calado
PMCID: PMC10441342  PMID: 37609190

Abstract

To increase antibody affinity against pathogens, positively selected GC-B cells initiate cell division in the light zone (LZ) of germinal centres (GCs). Among those, higher-affinity clones migrate to the dark zone (DZ) and vigorously proliferate by relying on oxidative phosphorylation (OXPHOS). However, it remains unknown how positively selected GC-B cells adapt their metabolism for cell division in the glycolysis-dominant, cell cycle arrest-inducing, hypoxic LZ microenvironment. Here, we show that microRNA (miR)-155 mediates metabolic reprogramming during positive selection to protect high-affinity clones. Transcriptome examination and mass spectrometry analysis revealed that miR-155 regulates H3K36me2 levels by directly repressing hypoxia-induced histone lysine demethylase, Kdm2a. This is indispensable for enhancing OXPHOS through optimizing the expression of vital nuclear mitochondrial genes under hypoxia. The miR-155-Kdm2a interaction is crucial to prevent excessive production of reactive oxygen species and apoptosis. Thus, miR-155-mediated epigenetic regulation promotes mitochondrial fitness in high-affinity clones, ensuring their expansion and consequently affinity maturation.

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