How heat shock inducesthe heat shock response (HSR) – a gene expression program encoding chaperones and other protein homeostasis (proteostasis) factors –remains an unresolved question in eukaryotic cell biology. Here we show that subcellular localization of the conserved J-protein Sis1 is a key regulator of the HSRin yeast. Under nonstress conditions, nucleoplasmic Sis1 promotes interaction between the chaperone Hsp70 and the transcription factor Hsf1to repress the HSR. Heat shock triggers Sis1 to localize to the nucleolar periphery and condense on the ER surface with the ribosome quality control complex. Sis1 recruits the proteasome to this spatial network.Through localization dynamics, Sis1 relaysthe condition of the proteome to Hsf1.Thus, the activation state of the HSR is built into spatial organization of the proteostasis network.