Mitochondrial contact site and cristae organizing system (MICOS) machinery supports heme biosynthesis by enabling optimal performance of ferrochelatase.


Journal

Redox biology
ISSN: 2213-2317
Titre abrégé: Redox Biol
Pays: Netherlands
ID NLM: 101605639

Informations de publication

Date de publication:
10 2021
Historique:
received: 12 07 2021
revised: 31 08 2021
accepted: 03 09 2021
pubmed: 14 9 2021
medline: 26 10 2021
entrez: 13 9 2021
Statut: ppublish

Résumé

Heme is an essential cofactor required for a plethora of cellular processes in eukaryotes. In metazoans the heme biosynthetic pathway is typically partitioned between the cytosol and mitochondria, with the first and final steps taking place in the mitochondrion. The pathway has been extensively studied and its biosynthetic enzymes structurally characterized to varying extents. Nevertheless, understanding of the regulation of heme synthesis and factors that influence this process in metazoans remains incomplete. Therefore, we investigated the molecular organization as well as the physical and genetic interactions of the terminal pathway enzyme, ferrochelatase (Hem15), in the yeast Saccharomyces cerevisiae. Biochemical and genetic analyses revealed dynamic association of Hem15 with Mic60, a core component of the mitochondrial contact site and cristae organizing system (MICOS). Loss of MICOS negatively impacts Hem15 activity, affects the size of the Hem15 high-mass complex, and results in accumulation of reactive and potentially toxic tetrapyrrole precursors that may cause oxidative damage. Restoring intermembrane connectivity in MICOS-deficient cells mitigates these cytotoxic effects. These data provide new insights into how heme biosynthetic machinery is organized and regulated, linking mitochondrial architecture-organizing factors to heme homeostasis.

Identifiants

pubmed: 34517185
pii: S2213-2317(21)00284-6
doi: 10.1016/j.redox.2021.102125
pmc: PMC8441213
pii:
doi:

Substances chimiques

Mitochondrial Proteins 0
Heme 42VZT0U6YR
Ferrochelatase EC 4.99.1.1

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

102125

Subventions

Organisme : NIGMS NIH HHS
ID : R35 GM131701
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM108975
Pays : United States
Organisme : NIEHS NIH HHS
ID : R33 ES025661
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM107001
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM089778
Pays : United States

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier B.V. All rights reserved.

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Auteurs

Jonathan V Dietz (JV)

Department of Biochemistry, University of Nebraska, Lincoln, NE, 68588, USA.

Mathilda M Willoughby (MM)

School of Chemistry and Biochemistry and School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA; Parker Petit Institute for Bioengineering and Biosciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Robert B Piel (RB)

Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA, 30602, USA.

Teresa A Ross (TA)

Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA, 30602, USA.

Iryna Bohovych (I)

Department of Biochemistry, University of Nebraska, Lincoln, NE, 68588, USA.

Hannah G Addis (HG)

Department of Chemistry and Biochemistry, College of Charleston, Charleston, SC, 29424, USA.

Jennifer L Fox (JL)

Department of Chemistry and Biochemistry, College of Charleston, Charleston, SC, 29424, USA.

William N Lanzilotta (WN)

Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA, 30602, USA.

Harry A Dailey (HA)

Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA, 30602, USA; Department of Microbiology, University of Georgia, Athens, GA, 30602, USA.

James A Wohlschlegel (JA)

Department of Biological Chemistry, University of California, Los Angeles, CA, 90095, USA.

Amit R Reddi (AR)

School of Chemistry and Biochemistry and School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA; Parker Petit Institute for Bioengineering and Biosciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Amy E Medlock (AE)

Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA, 30602, USA; Augusta University/University of Georgia Medical Partnership, Athens, GA, 30602, USA.

Oleh Khalimonchuk (O)

Department of Biochemistry, University of Nebraska, Lincoln, NE, 68588, USA; Nebraska Redox Biology Center, University of Nebraska, Lincoln, NE, 68588, USA; Fred & Pamela Buffett Cancer Center, Omaha, NE, 68198, USA. Electronic address: okhalimonchuk2@unl.edu.

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