A mitochondrial iron-responsive pathway regulated by DELE1

  • Mol Cell. 2023 Jun 15;83(12):2059-2076.e6. doi: 10.1016/j.molcel.2023.05.031.
Yusuke Sekine  1 Ryan Houston  2 Eva-Maria Eckl  3 Evelyn Fessler  3 Derek P Narendra  4 Lucas T Jae  3 Shiori Sekine  5
Affiliations
  • 1. Aging Institute, Department of Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15219, USA; Division of Endocrinology and Metabolism, Department of Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, USA.
  • 2. Aging Institute, Department of Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15219, USA.
  • 3. Gene Center and Department of Biochemistry, Ludwig-Maximilians-Universität München, 81377 Munich, Germany.
  • 4. Inherited Movement Disorders Unit, Neurogenetics Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20814, USA.
  • 5. Aging Institute, Department of Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15219, USA; Division of Cardiology, Department of Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, USA. Electronic address: [email protected].
Abstract

The heme-regulated kinase HRI is activated under heme/iron deficient conditions; however, the underlying molecular mechanism is incompletely understood. Here, we show that iron-deficiency-induced HRI activation requires the mitochondrial protein DELE1. Notably, mitochondrial import of DELE1 and its subsequent protein stability are regulated by iron availability. Under steady-state conditions, DELE1 is degraded by the mitochondrial matrix-resident protease LONP1 soon after mitochondrial import. Upon iron chelation, DELE1 import is arrested, thereby stabilizing DELE1 on the mitochondrial surface to activate the HRI-mediated integrated stress response (ISR). Ablation of this DELE1-HRI-ISR pathway in an erythroid cell model enhances cell death under iron-limited conditions, suggesting a cell-protective role for this pathway in iron-demanding cell lineages. Our findings highlight mitochondrial import regulation of DELE1 as the core component of a previously unrecognized mitochondrial iron responsive pathway that elicits stress signaling following perturbation of iron homeostasis.

Keywords
DELE1; HRI; LONP1; erythroid cells; integrated stress response; iron; mitochondria; mitochondrial import; mitochondrial proteostasis.
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