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PMID: 22245770 Published · ppublish English 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.

Hemin causes mitochondrial dysfunction in endothelial cells through promoting lipid peroxidation: the protective role of autophagy.

American journal of physiology. Heart and circulatory physiology ·Vol. 302 ·No. 7 ·2012-04-01 ·Pages H1394-409

Higdon AN, Benavides GA, Chacko BK, Ouyang X, Johnson MS, Landar A, Zhang J, Darley-Usmar VM

Abstract

The hemolysis of red blood cells and muscle damage results in the release of the heme proteins myoglobin, hemoglobin, and free heme into the vasculature. The mechanisms of heme toxicity are not clear but may involve lipid peroxidation, which we hypothesized would result in mitochondrial damage in endothelial cells. To test this, we used bovine aortic endothelial cells (BAEC) in culture and exposed them to hemin. Hemin led to mitochondrial dysfunction, activation of autophagy, mitophagy, and, at high concentrations, apoptosis. To detect whether hemin induced lipid peroxidation and damaged proteins, we used derivatives of arachidonic acid tagged with biotin or Bodipy (Bt-AA, BD-AA). We found that in cells treated with hemin, Bt-AA was oxidized and formed adducts with proteins, which were inhibited by α-tocopherol. Hemin-dependent mitochondrial dysfunction was also attenuated by α-tocopherol. Protein thiol modification and carbonyl formation occurred on exposure and was not inhibited by α-tocopherol. Supporting a protective role of autophagy, the inhibitor 3-methyladenine potentiated cell death. These data demonstrate that hemin mediates cytotoxicity through a mechanism which involves protein modification by oxidized lipids and other oxidants, decreased respiratory capacity, and a protective role for the autophagic process. Attenuation of lipid peroxidation may be able to preserve mitochondrial function in the endothelium and protect cells from heme-dependent toxicity.

MeSH Terms
Adenosine Triphosphate/metabolism Animals Antioxidants/pharmacology Autophagy/physiology Blotting, Western Cell Death/drug effects Cell Line Cell Survival/drug effects Cells, Cultured Chromatography, High Pressure Liquid Dogs Endothelial Cells/drug effects Energy Metabolism/drug effects Extracellular Fluid/metabolism Fluorescent Dyes Green Fluorescent Proteins/metabolism Hemin/pharmacology Indicators and Reagents Lipid Peroxidation/drug effects Membrane Potential, Mitochondrial/drug effects,physiology Mitochondrial Myopathies/chemically induced,pathology Protein Processing, Post-Translational/physiology
Chemicals
Antioxidants Fluorescent Dyes Indicators and Reagents Green Fluorescent Proteins Hemin Adenosine Triphosphate
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Higdon Ashlee N
Department of Pathology, Center For Free Radical Biology, University of Alabama at Birmingham, USA.
Benavides Gloria A
Chacko Balu K
Ouyang Xiaosen
Johnson Michelle S
Landar Aimee
Zhang Jianhua
Darley-Usmar Victor M
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Article Info
Journal
American journal of physiology. Heart and circulatory physiology
Abbr.
Am J Physiol Heart Circ Physiol
ISSN
1522-1539
Published
2012-04-01
Epub
2012-00-13
Pages
H1394-409
Language
English
Region
United States
NLM ID
100901228
PMCID
PMC3330785
Subset
IM
Grants
NINDS NIH HHS · R01 NS064090 · United States
NIEHS NIH HHS · ES/HL10167 · United States
NHLBI NIH HHS · R01-HL-096638 · United States
NINDS NIH HHS · R01-NS064090 · United States
NIDDK NIH HHS · DK75865 · United States
NIDDK NIH HHS · 1P30 DK 079337 · United States
NHLBI NIH HHS · R01 HL096638 · United States
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