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Some mitochondrial long noncoding RNAs (lncRNAs) are encoded by nuclear DNA, but the mechanisms that mediate their transport to mitochondria are poorly characterized. Using affinity RNA pull-down followed by mass spectrometry analysis, we found two RNA-binding proteins (RBPs), HuR (human antigen R) and GRSF1 (G-rich RNA sequence-binding factor 1), that associated with the nuclear DNA-encoded lncRNA  RMRP  and mobilized it to mitochondria. In cultured human cells, HuR bound  RMRP  in the nucleus and mediated its CRM1 (chromosome region maintenance 1)-dependent export to the cytosol. After  RMRP  was imported into mitochondria, GRSF1 bound  RMRP  and increased its abundance in the matrix. Loss of GRSF1 lowered the mitochondrial levels of  RMRP , in turn suppressing oxygen consumption rates and modestly reducing mitochondrial DNA replication priming. Our findings indicate that RBPs HuR and GRSF1 govern the cytoplasmic and mitochondrial localization of the lncRNA  RMRP , which is encoded by nuclear DNA but has key functions in mitochondria.

HuR and GRSF1 modulate the nuclear export and mitochondrial localization of the lncRNA RMRP