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The unfolded protein response (UPR) is a conserved mechanism that mitigates accumulation of unfolded proteins in the ER. The yeast UPR is subject to intricate post-transcriptional regulation, involving recruitment of the RNA encoding the Hac1 transcription factor to the ER and its unconventional splicing. To investigate the mechanisms underlying regulation of the UPR, we screened the yeast proteome for proteins that specifically interact with  HAC1  RNA. Protein microarray experiments revealed that  HAC1  interacts specifically with small  ras  GTPases of the Ypt family. We characterized the interaction of  HAC1  RNA with one of these proteins, the yeast Rab1 homolog Ypt1. We found that Ypt1 protein specifically associated  in vivo  with unspliced  HAC1  RNA. This association was disrupted by conditions that impaired protein folding in the ER and induced the UPR. Also, the Ypt1- HAC1  interaction depended on  IRE1  and  ADA5 , the two genes critical for UPR activation. Decreasing expression of the Ypt1 protein resulted in a reduced rate of  HAC1  RNA decay, leading to significantly increased levels of both unspliced and spliced  HAC1  RNA, and delayed attenuation of the UPR, when ER stress was relieved. Our findings establish that Ypt1 contributes to regulation of UPR signaling dynamics by promoting the decay of  HAC1  RNA, suggesting a potential regulatory mechanism for linking vesicle trafficking to the UPR and ER homeostasis.

The Yeast Rab GTPase Ypt1 Modulates Unfolded Protein Response Dynamics by Regulating the Stability of HAC1 RNA