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J. Biol. Chem., Vol. 282, Issue 45, 32821-32826, November 9, 2007

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Mitochondrial Swelling Impairs the Transport of Organelles in Cerebellar Granule Neurons^*

Allen Kaasik¹, Dzhamilja Safiulina, Vinay Choubey, Malle Kuum, Alexander Zharkovsky, and Vladimir Veksler^¶

From the Department of Pharmacology, Centre of Molecular and Clinical Medicine, University of Tartu, 51014 Tartu, Estonia, the INSERM, U-769, Châtenay-Malabry 92296, France, and the ^¶Université Paris-Sud, Châtenay-Malabry, 92296, France

Organelle transport in neuronal processes is central to the organization, developmental fate, and functions of neurons. Organelles must be transported through the slender, highly branched neuronal processes, making the axonal transport vulnerable to any perturbation. However, some intracellular structures like mitochondria are able to considerably modify their volume. We therefore hypothesized that swollen mitochondria could impair the traffic of other organelles in neurite shafts. To test this hypothesis, we have investigated the effects of mitochondrial swellers on the organelle traffic. Our data demonstrate that treatment of neurons with potassium ionophore valinomycin led to the fast time-dependent inhibition of organelle movement in cerebellar granule neurons. Similar inhibition was observed in neurons treated with the inhibitors of the mitochondrial respiratory chain, sodium azide and antimycin, which also induced swelling. No decrease in the motility of organelles was observed in cultures treated with inhibitors of ATP production or transport, oligomycin or bongkrekic acid, suggesting that inhibition of the ATP-generating activity itself without swelling does not affect the motility of organelles. The effect of swellers on the traffic was more important in thin processes, thus indicating the role of steric hindrance of swollen mitochondria. We propose that the size and morphology of the transported cargo is also relevant for seamless axonal transport and speculate that mitochondrial swelling could be one of the reasons for impaired organelle transport in neuronal processes.

Received for publication, March 16, 2007 , and in revised form, August 31, 2007.

^* This work was supported by grants from the Estonian Science Foundation (Grants 6227 and 7175), the European Community (contract MTKD-CT-2004-517176), the Centre of Molecular and Clinical Medicine, and the joint Estonian-French research program Parrot. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed: Dept. of Pharmacology, University of Tartu, Ravila 19, 51014 Tartu, Estonia, Tel.: 372-7374353; Fax: 372-7374352; E-mail: Allen.Kaasik{at}ut.ee.

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