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Molecular and Cellular Biology, January 2007, p. 411-425, Vol. 27, No. 2
0270-7306/07/$08.00+0     doi:10.1128/MCB.01391-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

A Cooperative Action of the ATP-Dependent Import Motor Complex and the Inner Membrane Potential Drives Mitochondrial Preprotein Import{triangledown}

Martin Krayl,1,2 Joo Hyun Lim,1,{dagger} Falk Martin,1 Bernard Guiard,3 and Wolfgang Voos1*

Institut für Biochemie und Molekularbiologie, Hermann-Herder-Str. 7, D-79104 Freiburg,1 Fakultät für Biologie, Universität Freiburg, Freiburg, Germany,2 Centre de Génétique Moléculaire, Laboratoire propre du CNRS associeté à l'Université Pierre et Marie Curie, 91190 Gif-sur-Yvette, France3

Received 28 July 2006/ Returned for modification 12 September 2006/ Accepted 20 October 2006

The import of mitochondrial preproteins requires an electric potential across the inner membrane and the hydrolysis of ATP in the matrix. We assessed the contributions of the two energy sources to the translocation driving force responsible for movement of the polypeptide chain through the translocation channel and the unfolding of preprotein domains. The import-driving activity was directly analyzed by the determination of the protease resistances of saturating amounts of membrane-spanning translocation intermediates. The ability to generate a strong translocation-driving force was solely dependent on the activity of the ATP-dependent import motor complex in the matrix. For a sustained import-driving activity on the preprotein in transit, an unstructured N-terminal segment of more than 70 to 80 amino acid residues was required. The electric potential of the inner membrane was required to maintain the import-driving activity at a high level. The electrophoretic force of the potential exhibited only a limited capacity to unfold preprotein domains. We conclude that the membrane potential increases the probability of a dynamic interaction of the preprotein with the import motor. Polypeptide translocation and unfolding are mainly driven by the inward-directed translocation activity based on the functional cooperation of the import motor components.

* Corresponding author. Mailing address: Institut für Biochemie und Molekularbiologie, Hermann-Herder-Str. 7, D-79104 Freiburg, Germany. Phone: 49-761-203-5280. Fax: 49-761-203-5261. E-mail: wolfgang.voos{at}biochemie.uni-freiburg.de.

{triangledown} Published ahead of print on 30 October 2006.

{dagger} Present address: Korea National Institute of Health, Dept. of Biomedical Sciences, Div. of Metabolic Diseases, Seoul, South Korea.

Molecular and Cellular Biology, January 2007, p. 411-425, Vol. 27, No. 2
0270-7306/07/$08.00+0     doi:10.1128/MCB.01391-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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