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Adaptation to changes in extracellular tonicity is essential for cell survival. However, severe or chronic hyperosmotic stress induces apoptosis, which involves cytochromec (Cytc ) release from mitochondria and subsequent apoptosome formation. Here, we show that angiogenin-induced accumulation of tRNA halves (or tiRNAs) is accompanied by increased survival in hyperosmotically stressed mouse embryonic fibroblasts. Treatment of cells with angiogenin inhibits stress-induced formation of the apoptosome and increases the interaction of small RNAs with released Cytc in a ribonucleoprotein (Cytc -RNP) complex. Next-generation sequencing of RNA isolated from the Cytc -RNP complex reveals that 20 tiRNAs are highly enriched in the Cytc -RNP complex. Preferred components of this complex are 5′ and 3′ tiRNAs of specific isodecoders within a family of isoacceptors. We also demonstrate that Cytc binds tiRNAsin vitro , and the pool of Cytc -interacting RNAs binds tighter than individual tiRNAs. Finally, we show that angiogenin treatment of primary cortical neurons exposed to hyperosmotic stress also decreases apoptosis. Our findings reveal a connection between angiogenin-generated tiRNAs and cell survival in response to hyperosmotic stress and suggest a novel cellular complex involving Cytc and tiRNAs that inhibits apoptosome formation and activity.

Angiogenin-Cleaved tRNA Halves Interact with Cytochrome c, Protecting Cells from Apoptosis during Osmotic Stress