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Brain Advance Access published online on March 31, 2009

Brain, doi:10.1093/brain/awp058
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© The Author (2009). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Review Article

Mitochondrial complex I deficiency: from organelle dysfunction to clinical disease

Felix Distelmaier1,2,3, Werner J.H. Koopman1, Lambertus P. van den Heuvel2, Richard J. Rodenburg2, Ertan Mayatepek3, Peter H.G.M. Willems1 and Jan A.M. Smeitink2

1 Department of Membrane Biochemistry, Nijmegen Centre for Molecular Life Sciences, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands 2 Department of Pediatrics, Nijmegen Center for Mitochondrial Disorders, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands 3 Department of General Pediatrics, Heinrich-Heine-University, Düsseldorf, Germany

Correspondence to: Dr F. Distelmaier, Department of General Pediatrics, University Children's Hospital, Heinrich-Heine-University, Moorenstr. 5, D-40225 Düsseldorf, Germany E-mail: felix.distelmaier{at}med.uni-duesseldorf.de

Mitochondria are essential for cellular bioenergetics by way of energy production in the form of ATP through the process of oxidative phosphorylation. This crucial task is executed by five multi-protein complexes of which mitochondrial NADH:ubiquinone oxidoreductase or complex I is the largest and most complicated one. During recent years, mutations in nuclear genes encoding structural subunits of complex I have been identified as a cause of devastating neurodegenerative disorders with onset in early childhood. Here, we present a comprehensive overview of clinical, biochemical and cell physiological information of 15 children with isolated, nuclear-encoded complex I deficiency, which was generated in a joint effort of clinical and fundamental research. Our findings point to a rather homogeneous clinical picture in these children and drastically illustrate the severity of the disease. In extensive live cell studies with patient-derived skin fibroblasts we uncovered important cell physiological aspects of complex I deficiency, which point to a central regulatory role of cellular reactive oxygen species production and altered mitochondrial membrane potential in the pathogenesis of the disorder. Moreover, we critically discuss possible interconnections between clinical signs and cellular pathology. Finally, our results indicate apparent differences to drug therapy on the cellular level, depending on the severity of the catalytic defect and identify modulators of cellular Ca2+ homeostasis as new candidates in the therapy of complex I deficiency.

Key Words: NADH:ubiquinone oxidoreductase deficiency; Leigh disease; ATP production; reactive oxygen species; treatment

Abbreviations: [ATP]M peak, bradykinin-induced peak increase in mitochondrial ATP concentration; BN-PAGE, blue-native polyacrylamide gel electrophoresis; Bk, bradykinin; [Ca]C peak, bradykinin-induced peak increase in cytosolic free Ca2+ concentration; [Ca]M peak, bradykinin-induced peak increase in mitochondrial free Ca2+ concentration; CM-DCF, 5-[and -6]-chloromethyl-2',7'-dichlorofluorescein; CI, complex I or NADH:ubiquinone oxidoreductase; ERCa, resting calcium content of the endoplasmic reticulum; ET, hydroethidine; OXPHOS, oxidative phosphorylation; ROS, reactive oxygen species; t1/2, half-time of the decay of the cytosolic free Ca2+ concentration following its peak increase in bradykinin-stimulated cells; {Delta}{psi}, mitochondrial membrane potential

Received December 8, 2008. Revised February 4, 2009. Accepted February 15, 2009.


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